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Chromatic rod vision—IX. A theoretical survey
Vision Rrs. Vol.
13, pp. 449455.
CHROMATIC
Pergamoa F'fess 1973. Printed inGreat BMaln
ROD VISION-IX.
A THEORETICAL
SURVEY’
BJ~RN STABELL and ULF STABELL Institute
of Psychology, University of Oslo, Norway (Received 31 May 1972)
EVER SINCEthe observation
of PURKINJE(1825) and AUBJZRT (1865), that all pigment colors, after dark adaptation and at low levels of illumination, appear colorless, it has been generally accepted that night vision is achromatic. In opposition to this view, however, all the principle hues of the spectrum have been observed at scotopic intensity levels (for a review see STABELL and STABELL, 1967a). Hence, if only rods function in scotopic vision-an assumption generally agreed-rods may mediate both achromatic and chromatic sensations. The hypothesis of rods as color receptors was apparently first suggested by EBBINGHAUS (1893) who assumed the photopigment of rods to be the yellow-blue substance postulated by HWNG (1878). Accordingly, rods were thought to mediate both blue and yellow sensations. The actions of light on visual purple and visual yellow, i.e. a blue-absorbing photoproduct of visual purple, were supposed to give rise to the sensations of yellow and blue, respectively. Influenced by the work of Ebbinghaus, KBNIG (1894) adopted the view that formation of visual yellow is a necessary condition for the experience of blue. In support of this he presented evidence indicating that the central fovea is blue-blind. In opposition to the hypothesis of Ebbinghaus, however, stimulation of visual purple was thought to give rise to an achromatic instead of a yellow sensation-a suggestion based on an experiment in which the absorption curve of visual purple was found to be strikingly similar to the visibility curve recorded at scotopic intensity levels, where sensation appeared achromatic. Half a century later WILLMER (1946)tried to explain color vision in terms of only one kind of cone and two kinds of rods; the “day-rods” and the ordinary dark-adapting rods. In agreement with the assumption of Ebbinghaus and Ksnig, the “blue” receptor was thought to function as such only when some degree of bleaching of the visual purple had occurred (WILLMER, 1946).The sensation of blue was thus attributed to the rods. As a consequence, he too, endeavoured to demonstrate the alleged blue-blindness of the rod-free area of the fovea. In harmony with the view of Ebbinghaus, K&g, and Willmer, that rods mediate the sensation of blue, LYTHGOE (1940) found the absorption curve and other properties of the regenerated substance of intermediate transient orange, to differ from those of the parent visual purple. He suggested that light might be the essential agent transforming the visual purple into the photosensitive substances responsible for day vision. Hence, the rod pigment was thought to change into the cone pigments during the process of light adaptation. Supporting electrophysiological evidence was presented by GRANIT (1963), who obtained modulator curves, with maxima on the blue side of 530 nm, from the guinea pig retina, 1 The Norwegian Research Council for Science and the Humanities supported this study financially. 449 V.R.1312-Q
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BJURNSTABELL ANDULFSTABELL
assumed to be without cones. As a possible explanation GRANIT (1963) pointed to Lythgoe’s transient orange as the blue modulator substance. Strong evidence against the hypotheses of Ebbinghaus, Ksnig, Wilimer, Lythgoe, and Granit, however, was presented by MARKS,DOBELLEand MACNXHOL (1964) and BROWN and WALD(I964), who measured the absorption spectra of single parafoveal receptors from the human retina, using a microspectrophotometer. Evidence was obtained for three types of cone pigments with maximum absorption in the violet, green-yellow, or yellow parts of the spectrum, together with the rhodopsin of the rods. Furthermore, WALD (1964, 19671, using a ~~rn~t~ng case of the two-color threshold method, presented evidence for the three kinds of cones within the rod-free area of the human fovea. At present, therefore, it is genera@ accepted that the sensation of hue in photopic vision is mediated by the absorbing pigments of the cones. Since only rods are assumed to function under scotopic conditions, however, the discovery of three types of cones does not preclude the possibility that photoproducts of rhodopsin provide the explanation of the chromatic aspect of night vision-somehow the rods must be thought to initiate the chromatic-related activity. The question is whether such activity is generated at the photochemicai or at a more central level in the visual system. WILLMER(1949), in a short note, appears to be the first to present evidence indicating that the chromatic-related activity originates centrally to the photochemical systems of the receptors, thus invalidating the photochem~cal explanation. using the method of simultaneous contrast an initially achromatic test field appeared bluish at an intensity below the specific threshold level when a chromatic inducing field was presented. Presupposing that the test field activated rods only, the sensation of blue was assumed to result from interacting rod and cone pathways. However, since the specific threshold curve starts rising at about the break-point of the dark adaptation curve (LIE, 1963), cones may be activated by stimuli of intensities between the break-point and the specific threshold. Hence the criterion of specific threshold, used by WKLNER (1949), does not ensure that only rods were test-stimulated. The question, therefore, remains whether rods or cones initiated the sensation of blue. Furthermore, since also the inducing field probably activated both rods and cones, the sensation of blue observed might be attributed to cone-cone, cone-rod, or rod-rod interaction, Three lines of evidence, however, support the hypothesis of W~~lmerthat rods and cones may interact to produce sensation of hue: (1) Using the methods of successive and simultaneous contrast, chromatic colors may be observed at intensities throughout the photochromatic interval (STABELLand STABELL, 1965, 1967b, 1968b, 1972d, 1973b; STABELL,B., 1967). (2) The scotopic contrast hue changes and becomes dependent on waveie~~gth of teststimulation when test-intensity increases above the specific threshold. The results suggest that the combined effect af simultaneous chromatic rod and cone activities is a kind of color mixing process (STABELL,U., 1967; STABELL,B., 1969; STaBELLand STABELL,1969a, 1969~). (3) The specific threshold may fall to lower intensity levels when a scotopic rod component is super~mposed~ snggest~ng that rod activity may faciiibte chromatic-related cone activity (STABELLand STABELL,1971a, 1971d). The present survey of chromatic rod vision is restricted to the first line of evidence where rods aione are thought to be test-stimulated. The evidence indicates that (a) selective chromatic stimulation of cones creates a disposition for a hue-retated response, and (b) the
Chromatic Rod Vision-K
A Theoretical Survey
response is triggered centrally to the photochemical initiated in the rods.
451
systems of the receptors by impulses
Evidence in favour of (a) (1) The smallest quantity of light of pre-stimulation which may produce a sensation of hue at scotopic intensity levels, stands in unique relation to the intensity level of the specific threshold, independently of factors influencing the magnitude of the photochromatic interval (STABELL,B., 1968). (2) Scotopic hue is closely related to additive opponent hue, indicating that it reflects the ratio of primary hue-related processes of pre-stimulation (STABELLand STABELL,1971e, 1972b, 1972c, 1973a). Assuming that the Principle of Univariance is valid, it follows that the hue discrimination curve depends on interaction between responses from different types of receptors (cf. STABELL and STABELL,1971b). Hence, the evidence presented suggests that cones produce the disposition for the hue-related activity in scotopic vision. Evidence in farour of(b)
(1) The absorption curve of rhodopsin shows a close correspondance to the spectral sensitivity curve of scotopic vision- there is no evidence of any contribution of cone function to the visual process (cf. WALD and BROWN,1958). (2) The absolute and color threshold generally coincide during dark adaptation at scotopic intensity levels, irrespective of pre- and test-stimulation variables. The sensation of hue may be observed down to the absolute threshold of dark adapted rods (STABELLand STABELL,1967b). (3) The scotopic contrast hue is independent of the wavelength used in the test (STABELL and STABELL,1968b, 1972b). (4) The scotopic hue changes, and becomes dependent on the wavelength of teststimulation, when the test intensity increases above the specific threshold (STABELL,B., 1969 ; STABELLand STABELL,1972d). (5) Duration of scotopic hue is a function of the photochromatic interval (STABELLand STABELL,1969b). In conclusion then, there seems to be well-founded evidence in favour of the assumption that scotopic contrast hue results from interaction between cone and rod activities and, therefore, probably originates centrally to the photochemical systems of the receptors. Consequently, the photochemical explanation of scotopic contrast hue may be excluded. Furthermore, the evidence appears to contradict the prevailing hypothesis of independence between rod and cone activities suggested by HECHT, 1937; ALPERN, 1965; RUSHTON,1965; IKEDAand URAKUBO,1969; BROWN,METZ and YOHMAN,1969; WESTHEIMER,1970). Evidence for a functional antagonism between rod and cone activities has accumulated (cf. GRANIT, 1947; DODT and JESSEN,1961; LIE, 1963 ; WILLMER,1965 ; GOURASand LINK, 1965; BROWNand MURAKAMI,1968; FRUMKES,SEKULERand REISS,1972), but none of these studies appears to have a direct bearing on the hypothesis that rods and cones may interact to produce hue sensations. A few electrophysiological studies, however, provide evidence indicating that cells, which in photopic states are supposed to mediate the sensation of hue may, at scotopic levels of stimulation, receive their inputs from rods (GRANIT, 1963; MITARAI, SVAETICHIN,VALLECALLE,FATEHCHAND,VILLEGASand LAUFER, 1961; WIESEL and HUBEL, 1966). This gives a physiological basis for chromatic rod vision. In photopic
452
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ULFSTABELL
vision the color cells appear to receive inputs from two antagonistic sets of cone connections, one excitatory and the other inhibitory with maxima of excitation and inhibition approximately in the red and green or yellow and blue regions of the spectrum (cf. ABRAMOV,1968). This supports the opponent color theory presented by HERING (1878). Hence, Hering’s theory seems to offer the best basis for an interpretation of scotopic contrast hue. Taking into account additional electrophysiological knowledge, which indicates that photopic hue sensation is determined by the relative activity rates of the different types of spectrally opponent cell (cf. DE VALOIS,ABRAMOV and JACOBS,1966), an explanation of scotopic hue might be based on the following assumptions (cf. STABELLand STABELL,1971e). (I) Hue, both in scotopic and photopic vision, is encoded in the visual pathway by the relative activity rates of the different types of spectrally opponent cells. (2) The opponent cells are activated to about the same degree, producing an achromatic sensation when the eye, in a completely dark-adapted state, is stimulated at scotopic intensity levels. (3) Following complete dark adaptation, selective chromatic pre-stimulation of the three types of cones changes the sensitivity of the opponent cells in proportion as they are activated. (4) Upon test-stimulation at scotopic intensity levels, the change in sensitivity of the opponent cells produced by the pre-stimulation affects the impulse pattern initiated in the rods and thus changes the relative activity rates of the opponent cells, giving rise to a hue approximately opponent to the hue of pre-stimulation. Scotopic hue of simultaneous contrast might be explained on the same principles. Accordingly, selective chromatic stimulation of the three types of cones of the inducing field may be thought to change the relative sensitivity of the opponent cells associated with the test area, producing a disposition for scotopic hue triggered upon test-stimulation of rods. In support of these assumptions, the scotopic contrast hue has been shown to be closely related to the additive opponent hue (cf. STABELLand STABELL,1971e), indicating that it basically reflects the ratio of primary hue-related processes of pre-stimulation. However, the scotopic hue was found to be displaced somewhat towards red and blue relative to the opponent hue, suggesting that the points of equilibrium of the red-green substance (where no disposition for red or green is produced by pre-stimulation) are displaced towards wavelengths that have a red valence, while the points of equilibrium of the yellow-blue substance (where no disposition for yellow or blue is produced) are displaced towards wavelengths that have a blue valence. Accordingly, primary yellow and blue pre-stimulation produced, respectively, intermediate scotopic hues of violet and orange, while primary green and red produced purple and blue-green, respectively. Since intermediate hues are thought to depend on processes in both the red-green and yellow-blue substances, each primary must induce an increment in the two response pairs. Hence, it follows, on the basis of Hering’s color theory (cf. HERING,1964), that each primary also produces a decrement in the two substances. Consequently, it may be concluded that pre-stimulation with a primary hue involves each of the primary hue-related processes, a suggestion in harmony with electrophysiological evidence, which indicates that every light of the spectrum, including the primaries, may change the sensitivity of each type of opponent cell (cf. STABELLand STABELL,1972a). The displacement of the equilibrium points further implies that stimulation with orange or violet light may produce an increment of red, instead of green as would be expected on
Chromatic Rod Vision-IX. A Theoretical Survey
453
the basis of Hering’s opponent theory. Purple and blue-green on the other hand may produce an increment of blue instead of yellow. Since increments of red and blue are thought to reflect green- and yellow-related activities, respectively, stimulation with orange or violet light may be thought to activate a green-related process producing the disposition for red, while stimulation with blue-green or purple may activate a yellow-related process producing the disposition for blue. The disposition for scotopic hue produced by chromatic stimulation is, however, thought to change gradually during dark adaptation toward a mid-valued state, where the antagonistic processes are of equal magnitude. Test-stimulation in this neutral state, at intensities within the photochromatic interval, produces an achromatic sensation, irrespective of teststimulation variables. Accordingly, rod impulses are assumed to trigger the disposition for scotopic hue without changing the ratio of the hue-related processes initiated, and may thus be thought of as a constant stimulus, regardless of test variables. The scotopic contrast hue has thus been assumed to be controlled basically by the disposition produced by chromatic stimulation of cones. In conformity with the suggestion, the scotopic hue has been found to be broadly invariant of wavelength and intensity of test-stimulation (STABELLand STABELL, 1971b, 1972d). The question remains, however, whether it is bleaching or light signals from cones that cause the change in sensitivity of the opponent cells. At present, evidence seems to favour the second alternative (STABELL,B., 1968; STABELLand STABELL,1971~). It has been shown, for example, that scotopic hue may remain visible for more than one hour while cone pigments are thought to regenerate within a few minutes (cf. RUSHTON,1957). CONCLUSION There appears to be well-founded evidence in favour of the assumption that scotopic contrast hue originates centrally to the photochemical systems of the receptors, and results from interaction between cone and rod activities. Selective chromatic stimulation of the three types of cones is assumed to change the relative sensitivity of the opponent cells, producing a disposition for scotopic hue which is triggered upon test-stimulation of rods. Rods may thus be thought to mediate every hue of the spectrum depending on the disposisition of the opponent cells. The achromatic aspect of night vision is observed only under conditions where the opponent cells are in a neutral state. In opposition to Helmholtz’s color theory (HELMHOLTZ, 1896) it is thus suggested that receptors that are morphologically and biochemically identical may give rise to different sensations of hue. REFERENCES ABRAMOV, I. (1968).Further analysis of the responses of LGN cells. J. opt. SOC.Am. S&574-579. ALPERN, M. (1965).Rod-cone independencein the after-flasheffect. J. Physiol., Land. 176,462-472. AUBERT,H. (1865) Physiologic der Netzhaut. Morgenstern, Breslau.
BROWN,J. L., METZ,J. W. and YOHMAN,J. R. (1969). Test of scotopic suppression of the photopic process. J. opt. Sot. Am. 59, 1677-1678. BROWN, K. T. and MURAKAMI, M. (1968). Rapid effects of light and dark adaptation upon the receptive field organization of S-potentials and late receptor potentials. Vision Res. 8, 1145-1171. BROWN, P. K. and WALD, G. (1964). Visual pigments in single rods and cones of the human retina. Science, N. Y. 144,45-52. DE VALOI~,R. L., ABRAMOV, I. and JACOBS,G. H. (1966). Analysis of response patterns of LGN cells. J. opr. Sot. Am. 56,966-977. DODT, E. and JESSEN,K. H. (1960). Depression of cone sensitivity during dark-adaptation. Experientiu 16, 205-206. EBBINGHAUS, H. (1893). Theorie des Farbensehens. 2. Psychol. Physiof. Sinnesorg. 5, 145-238.
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BJBRNSTABELLAND ULF
STABELI.
FFXJM~_ T. E., SEKULFX,M. D, and Russ, E. H. (1972). Rod-cone interaction in human scotopic vision. Science, N. Y. 175,913-914. GOURAS,P. and LMK, K. (1966). Rod and cone interaction in dark-adapted monkey ganglioncells. f, Physiat.,
Land. l&$,499-510.
GRAN~T, R. (1963). Sensory &fechanismsof the Retina. Hafner, New York. HECHT, S. (1937). Rods, cones, and the chemical basis of vision. pi~J~+riol. Ret>. 17, 239-290. HELMHOLTZ,H. VON (1896). Handbuch der physiologischen Optik. Leopold Voss, Hamburg and Leipzig. HERING, E. (1878). Zur Lehre cum Lkhtsinne. Carl Gerold Sohn’s, Wien. HERING,E. (1964). Ouflines ofa jrbeory ofthe Light Sense (Translated by L. M. HURVICHand D. JAMESON), Harvard Univ. Press, Cambridge, Mass. IKEDA, M. and URAKUBO,M. (1969). Rod-cone interrelation. J. opt, Sot. Am. 59, 217-222. K.ONIG,A. (1894). uher den menschhchen Sehpurpur und seine Bedeutung fiir das Sehen. SirrBer. Pt-euss. Akad. Wk. 2, Halbhd., 577-598. LIE,I,(1963). Dark adaptation and the photochromatic interval Docunrenia ophth. 17,41 t-510. L~TH~OE, R. f. (1940). The mechanism of dark adaptation. A critical resumg. Br, .K Uphth~~~ 24,21-43, MARKS, W. B., Dom~~x+ W. H. and MacNr~o~~ E. F. (1964). Visual pigments of singIe primate cones. Science, N.Y. 143,1181-1182. Mrr~linr, G., S~AFTIC~N, G., VALLECALLE, E.,FATEHCHAND,R., VUEGAS, J. and LAUFER,M. (1961). Glianeuron interaction and adaptational mechanisms of the retina. In Neurophysiofogieund Psychophysik des visueilen Systems (edited by R. JUNG and H. KORNHUBER),pp. 463-481, Springer, Berlin. PURKINIE,J. (1825). Beobachtuttgen und Versuche zur Physiologic der Sinne. Neue Beitriige _wr Kenntniss des Sehens in subjectiver Hindsicht. Vol. 2. Reimer, Berlin. RUSHTON,W. A. H. (1957). Physical measurements of cone pigment in the living human eye. Nature, Land. 179,571-573. RUSHTON,W. A. H. (1965). The Ferrier Lecture: visual adaptation PKJC. R. Sot., B. 162, 20-46. STABELL,B. (1967). Rods as color receptors in scotopic vision. Scud. J. Psycho!. 8, 132-138. STABELL,B. (1968). Rod vision as chromatic vision. Scund. J. Psycho!. 9, 282-288. STABE~L,B. (1969). Transition from rod to cone vision. I. Simultaneous contrast. Seand. J. Psychol. IO,
61-644. STABELL, B. and STABELL, U. (1967a). Night vision as chromatic vision. Stand J. Psucfraf. 8,145-149.
STMW_L,B. and STABELL,IJ. (1967b). Color threshold ~~ure~~ts
in scotopic vision I. Pre-stimulation varied. SCQZXZ.T. Psychol. 8,268-272. STA~)ELL,B. and STABU~, IJ. (1969a). Transition from rod to cone vision. II. Successive contrast. Semd. J.
Psychol. l&137-139. STABELL,3. and STABELL,W. (1969b). Chromatic rod and cone activities as a function of the photochromatic interval. Scund. J. Psycho/. 10, 215-219. STABELL,B. and STABELL,IJ. (1971a). Facilitation of chromatic cone activity by rod activity. I. Red-related cone activity. Stand. J. Psychal. If, 99-105. STABELL, B. and STABELL, W. (197lb). Chromatic rod vision I. Wavelength of test-stimulation varied. Stand. J. Psychol. 12, 175-178. STABELL,B. and STABELL,U. (1972a). Chromatic rod vision. III. Duration of pro-stimulation varied. Scann! J. Psychof. 13, 136-140. STABELL,B. and STABELL,W. (1972b). Chromatic rod vision. IV. Time between pre- and test-stimulation varied. Scatuf. J. Psychol. 13,141-W. ST~BELL, 8. and STABELL, Il. (1973a). Chromatic rod vision. VII. Intensity of pre-stimulation varied. Stand. J. PsychoA 14. STABELL, W. fl967f. Rods as color receptors in photopic vision Stand. J. Psycho{. % 139-144. STA~ELL, U. and STABEJ_L, B. (1965). Rods as color receptors. Stand, f. Psycfiof. 6, 195-260. STABELL,U. and STABELL,B. (1968a). Color threshold measurements in scotopic vision. II. Test-stimulation varied. Stand. J. Ps~+chol. 9,129-132. STABELL,U. and STABELL,B. (1968b). Color threshold measurements in scotopic vision. III. Simultaneous color contrast. Scond. J. Psychok 9, 133-137. STABELL,U. and STABELL,B. (1969c). Transition from rod to cone vision. III. Successive contrast anew.
Stand. J. Psycho/. 10,140-144.
STABELL,IJ. and STABELL,B. (1971c). Duration of scotopic contrast hue. Stand. J. Psychol. 12, 106-112. STABELL,U. and STABELL,B, (1971d). Facilitation of chromatic cone activity by rod activity. II. Variation of chromatic-related cone activity, Scund. S. Psychol. 12, 168-174. STABELL, U. and STABELL, B. (197le). Chromatic rod vision. II. Wavelength of pre-stimulation varied.
Stand. J. Psychof. 12,282~288. STABELL,W. and STABELL, B. (1972~). Chromatic rod vision. V. Retinal location of stimulation varied. Sfnltb. J. P&WA 13. STAEELL, U. andSTABELL,B. (1972df. Chromatic rod vision. Vf, Intensity of Tut-stimulation varied. Stand, J. Psyckoi. 13.
Chromatic
Rod Vision-IX.
A Theoretical Survey
45.5
U. and STABELL,B. (1973b). Chromatic rod vision. VIII: Simultaneous contrast. &and. J. P&rol. 14. WALD, G. (1964). The receptors of human color vision. Science, N. Y. 145, 1007-1017. WALD, G. (1967). Blue-blindness in the normal fovea. J. opt. Sot. Am. 57, 1289-1301. WALD, G. and BROWN, P. K. (1958). Human rhodopsin. Science, N. Y. 127,222-226. WESTHEIMER, G. (1970). Rod-cone independence for sensitizing interaction in the human retina. J. Physiol., Land. 206, 109-116. WIESEL,T. N. and HUBEL,D. H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J. Neurophysiol. 29, 1115-l 156. WILLMER,E. N. (1946). Retinal Structure and Colour Vision. Cambridge University Press, Cambridge. WILLMER.E. N. (1949). Low threshold rods and the vercevtion of blue. J. Physiol., Lmd. 11. 17P. WILLMER;E. N. ‘(1965). Duality in the retina. In Cilour -Vision: Physiology-and kxperime&l PsychoIogy (edited by A. V. S. DE REUCK and J. KNIGHT), pp. 89-109. Churchill, London. STABELL,
Abstract-Theories of rods as color receptors are reviewed and evaluated. There appears to be well-founded evidence in favour of the hypothesis that rods and cones may interact to produce sensation of hue. Accordingly it is suggested that light signals from cones may change the relative sensitivity of the spectrally opponent cells, producing a disposition for scotopic hue that is triggered upon test-stimulation of rods. R&sumt!-On passe en revue et on discute les theories qui confient aux bltonnets un role dans la reception coloree. Des arguments sdrieux semblent en faveur de l’hypoth&se dune interaction des batonnets et des cones pour produire la sensation de tonalitd. On suggere done que les signaux lumineux des cbnes peuvent changer la sensibilite relative des cellules spectralement antagonistes, ce qui permet une tonalitd scotopique par stimulation des batonnets. Zusammenfasstmg-Theorien, die Stabchen als Farbrezeptoren betrachten, wurden iiberpriift und abgeschatzt. Es scheinen wohlbegriindete Anhaltspunkte dafiir zu sprechen da8 Stgbchen und Zapfen bei der Farbempfindung zusammenwirken. Dementsprechend wird vermutet, daD lichterregte Zapfen die relative Emptindlichkeit der spektral entgegengesetzten Zellen verandern konnen, indem sie die Farbemptindung im skotopischen Bereich so voreinstellen, da6 sie durch einen Testreiz der Stabchen au&&t wird.
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13, pp. 449455.
CHROMATIC
Pergamoa F'fess 1973. Printed inGreat BMaln
ROD VISION-IX.
A THEORETICAL
SURVEY’
BJ~RN STABELL and ULF STABELL Institute
of Psychology, University of Oslo, Norway (Received 31 May 1972)
EVER SINCEthe observation
of PURKINJE(1825) and AUBJZRT (1865), that all pigment colors, after dark adaptation and at low levels of illumination, appear colorless, it has been generally accepted that night vision is achromatic. In opposition to this view, however, all the principle hues of the spectrum have been observed at scotopic intensity levels (for a review see STABELL and STABELL, 1967a). Hence, if only rods function in scotopic vision-an assumption generally agreed-rods may mediate both achromatic and chromatic sensations. The hypothesis of rods as color receptors was apparently first suggested by EBBINGHAUS (1893) who assumed the photopigment of rods to be the yellow-blue substance postulated by HWNG (1878). Accordingly, rods were thought to mediate both blue and yellow sensations. The actions of light on visual purple and visual yellow, i.e. a blue-absorbing photoproduct of visual purple, were supposed to give rise to the sensations of yellow and blue, respectively. Influenced by the work of Ebbinghaus, KBNIG (1894) adopted the view that formation of visual yellow is a necessary condition for the experience of blue. In support of this he presented evidence indicating that the central fovea is blue-blind. In opposition to the hypothesis of Ebbinghaus, however, stimulation of visual purple was thought to give rise to an achromatic instead of a yellow sensation-a suggestion based on an experiment in which the absorption curve of visual purple was found to be strikingly similar to the visibility curve recorded at scotopic intensity levels, where sensation appeared achromatic. Half a century later WILLMER (1946)tried to explain color vision in terms of only one kind of cone and two kinds of rods; the “day-rods” and the ordinary dark-adapting rods. In agreement with the assumption of Ebbinghaus and Ksnig, the “blue” receptor was thought to function as such only when some degree of bleaching of the visual purple had occurred (WILLMER, 1946).The sensation of blue was thus attributed to the rods. As a consequence, he too, endeavoured to demonstrate the alleged blue-blindness of the rod-free area of the fovea. In harmony with the view of Ebbinghaus, K&g, and Willmer, that rods mediate the sensation of blue, LYTHGOE (1940) found the absorption curve and other properties of the regenerated substance of intermediate transient orange, to differ from those of the parent visual purple. He suggested that light might be the essential agent transforming the visual purple into the photosensitive substances responsible for day vision. Hence, the rod pigment was thought to change into the cone pigments during the process of light adaptation. Supporting electrophysiological evidence was presented by GRANIT (1963), who obtained modulator curves, with maxima on the blue side of 530 nm, from the guinea pig retina, 1 The Norwegian Research Council for Science and the Humanities supported this study financially. 449 V.R.1312-Q
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BJURNSTABELL ANDULFSTABELL
assumed to be without cones. As a possible explanation GRANIT (1963) pointed to Lythgoe’s transient orange as the blue modulator substance. Strong evidence against the hypotheses of Ebbinghaus, Ksnig, Wilimer, Lythgoe, and Granit, however, was presented by MARKS,DOBELLEand MACNXHOL (1964) and BROWN and WALD(I964), who measured the absorption spectra of single parafoveal receptors from the human retina, using a microspectrophotometer. Evidence was obtained for three types of cone pigments with maximum absorption in the violet, green-yellow, or yellow parts of the spectrum, together with the rhodopsin of the rods. Furthermore, WALD (1964, 19671, using a ~~rn~t~ng case of the two-color threshold method, presented evidence for the three kinds of cones within the rod-free area of the human fovea. At present, therefore, it is genera@ accepted that the sensation of hue in photopic vision is mediated by the absorbing pigments of the cones. Since only rods are assumed to function under scotopic conditions, however, the discovery of three types of cones does not preclude the possibility that photoproducts of rhodopsin provide the explanation of the chromatic aspect of night vision-somehow the rods must be thought to initiate the chromatic-related activity. The question is whether such activity is generated at the photochemicai or at a more central level in the visual system. WILLMER(1949), in a short note, appears to be the first to present evidence indicating that the chromatic-related activity originates centrally to the photochemical systems of the receptors, thus invalidating the photochem~cal explanation. using the method of simultaneous contrast an initially achromatic test field appeared bluish at an intensity below the specific threshold level when a chromatic inducing field was presented. Presupposing that the test field activated rods only, the sensation of blue was assumed to result from interacting rod and cone pathways. However, since the specific threshold curve starts rising at about the break-point of the dark adaptation curve (LIE, 1963), cones may be activated by stimuli of intensities between the break-point and the specific threshold. Hence the criterion of specific threshold, used by WKLNER (1949), does not ensure that only rods were test-stimulated. The question, therefore, remains whether rods or cones initiated the sensation of blue. Furthermore, since also the inducing field probably activated both rods and cones, the sensation of blue observed might be attributed to cone-cone, cone-rod, or rod-rod interaction, Three lines of evidence, however, support the hypothesis of W~~lmerthat rods and cones may interact to produce sensation of hue: (1) Using the methods of successive and simultaneous contrast, chromatic colors may be observed at intensities throughout the photochromatic interval (STABELLand STABELL, 1965, 1967b, 1968b, 1972d, 1973b; STABELL,B., 1967). (2) The scotopic contrast hue changes and becomes dependent on waveie~~gth of teststimulation when test-intensity increases above the specific threshold. The results suggest that the combined effect af simultaneous chromatic rod and cone activities is a kind of color mixing process (STABELL,U., 1967; STABELL,B., 1969; STaBELLand STABELL,1969a, 1969~). (3) The specific threshold may fall to lower intensity levels when a scotopic rod component is super~mposed~ snggest~ng that rod activity may faciiibte chromatic-related cone activity (STABELLand STABELL,1971a, 1971d). The present survey of chromatic rod vision is restricted to the first line of evidence where rods aione are thought to be test-stimulated. The evidence indicates that (a) selective chromatic stimulation of cones creates a disposition for a hue-retated response, and (b) the
Chromatic Rod Vision-K
A Theoretical Survey
response is triggered centrally to the photochemical initiated in the rods.
451
systems of the receptors by impulses
Evidence in favour of (a) (1) The smallest quantity of light of pre-stimulation which may produce a sensation of hue at scotopic intensity levels, stands in unique relation to the intensity level of the specific threshold, independently of factors influencing the magnitude of the photochromatic interval (STABELL,B., 1968). (2) Scotopic hue is closely related to additive opponent hue, indicating that it reflects the ratio of primary hue-related processes of pre-stimulation (STABELLand STABELL,1971e, 1972b, 1972c, 1973a). Assuming that the Principle of Univariance is valid, it follows that the hue discrimination curve depends on interaction between responses from different types of receptors (cf. STABELL and STABELL,1971b). Hence, the evidence presented suggests that cones produce the disposition for the hue-related activity in scotopic vision. Evidence in farour of(b)
(1) The absorption curve of rhodopsin shows a close correspondance to the spectral sensitivity curve of scotopic vision- there is no evidence of any contribution of cone function to the visual process (cf. WALD and BROWN,1958). (2) The absolute and color threshold generally coincide during dark adaptation at scotopic intensity levels, irrespective of pre- and test-stimulation variables. The sensation of hue may be observed down to the absolute threshold of dark adapted rods (STABELLand STABELL,1967b). (3) The scotopic contrast hue is independent of the wavelength used in the test (STABELL and STABELL,1968b, 1972b). (4) The scotopic hue changes, and becomes dependent on the wavelength of teststimulation, when the test intensity increases above the specific threshold (STABELL,B., 1969 ; STABELLand STABELL,1972d). (5) Duration of scotopic hue is a function of the photochromatic interval (STABELLand STABELL,1969b). In conclusion then, there seems to be well-founded evidence in favour of the assumption that scotopic contrast hue results from interaction between cone and rod activities and, therefore, probably originates centrally to the photochemical systems of the receptors. Consequently, the photochemical explanation of scotopic contrast hue may be excluded. Furthermore, the evidence appears to contradict the prevailing hypothesis of independence between rod and cone activities suggested by HECHT, 1937; ALPERN, 1965; RUSHTON,1965; IKEDAand URAKUBO,1969; BROWN,METZ and YOHMAN,1969; WESTHEIMER,1970). Evidence for a functional antagonism between rod and cone activities has accumulated (cf. GRANIT, 1947; DODT and JESSEN,1961; LIE, 1963 ; WILLMER,1965 ; GOURASand LINK, 1965; BROWNand MURAKAMI,1968; FRUMKES,SEKULERand REISS,1972), but none of these studies appears to have a direct bearing on the hypothesis that rods and cones may interact to produce hue sensations. A few electrophysiological studies, however, provide evidence indicating that cells, which in photopic states are supposed to mediate the sensation of hue may, at scotopic levels of stimulation, receive their inputs from rods (GRANIT, 1963; MITARAI, SVAETICHIN,VALLECALLE,FATEHCHAND,VILLEGASand LAUFER, 1961; WIESEL and HUBEL, 1966). This gives a physiological basis for chromatic rod vision. In photopic
452
Bmw
Sc4m.f.~~~
ULFSTABELL
vision the color cells appear to receive inputs from two antagonistic sets of cone connections, one excitatory and the other inhibitory with maxima of excitation and inhibition approximately in the red and green or yellow and blue regions of the spectrum (cf. ABRAMOV,1968). This supports the opponent color theory presented by HERING (1878). Hence, Hering’s theory seems to offer the best basis for an interpretation of scotopic contrast hue. Taking into account additional electrophysiological knowledge, which indicates that photopic hue sensation is determined by the relative activity rates of the different types of spectrally opponent cell (cf. DE VALOIS,ABRAMOV and JACOBS,1966), an explanation of scotopic hue might be based on the following assumptions (cf. STABELLand STABELL,1971e). (I) Hue, both in scotopic and photopic vision, is encoded in the visual pathway by the relative activity rates of the different types of spectrally opponent cells. (2) The opponent cells are activated to about the same degree, producing an achromatic sensation when the eye, in a completely dark-adapted state, is stimulated at scotopic intensity levels. (3) Following complete dark adaptation, selective chromatic pre-stimulation of the three types of cones changes the sensitivity of the opponent cells in proportion as they are activated. (4) Upon test-stimulation at scotopic intensity levels, the change in sensitivity of the opponent cells produced by the pre-stimulation affects the impulse pattern initiated in the rods and thus changes the relative activity rates of the opponent cells, giving rise to a hue approximately opponent to the hue of pre-stimulation. Scotopic hue of simultaneous contrast might be explained on the same principles. Accordingly, selective chromatic stimulation of the three types of cones of the inducing field may be thought to change the relative sensitivity of the opponent cells associated with the test area, producing a disposition for scotopic hue triggered upon test-stimulation of rods. In support of these assumptions, the scotopic contrast hue has been shown to be closely related to the additive opponent hue (cf. STABELLand STABELL,1971e), indicating that it basically reflects the ratio of primary hue-related processes of pre-stimulation. However, the scotopic hue was found to be displaced somewhat towards red and blue relative to the opponent hue, suggesting that the points of equilibrium of the red-green substance (where no disposition for red or green is produced by pre-stimulation) are displaced towards wavelengths that have a red valence, while the points of equilibrium of the yellow-blue substance (where no disposition for yellow or blue is produced) are displaced towards wavelengths that have a blue valence. Accordingly, primary yellow and blue pre-stimulation produced, respectively, intermediate scotopic hues of violet and orange, while primary green and red produced purple and blue-green, respectively. Since intermediate hues are thought to depend on processes in both the red-green and yellow-blue substances, each primary must induce an increment in the two response pairs. Hence, it follows, on the basis of Hering’s color theory (cf. HERING,1964), that each primary also produces a decrement in the two substances. Consequently, it may be concluded that pre-stimulation with a primary hue involves each of the primary hue-related processes, a suggestion in harmony with electrophysiological evidence, which indicates that every light of the spectrum, including the primaries, may change the sensitivity of each type of opponent cell (cf. STABELLand STABELL,1972a). The displacement of the equilibrium points further implies that stimulation with orange or violet light may produce an increment of red, instead of green as would be expected on
Chromatic Rod Vision-IX. A Theoretical Survey
453
the basis of Hering’s opponent theory. Purple and blue-green on the other hand may produce an increment of blue instead of yellow. Since increments of red and blue are thought to reflect green- and yellow-related activities, respectively, stimulation with orange or violet light may be thought to activate a green-related process producing the disposition for red, while stimulation with blue-green or purple may activate a yellow-related process producing the disposition for blue. The disposition for scotopic hue produced by chromatic stimulation is, however, thought to change gradually during dark adaptation toward a mid-valued state, where the antagonistic processes are of equal magnitude. Test-stimulation in this neutral state, at intensities within the photochromatic interval, produces an achromatic sensation, irrespective of teststimulation variables. Accordingly, rod impulses are assumed to trigger the disposition for scotopic hue without changing the ratio of the hue-related processes initiated, and may thus be thought of as a constant stimulus, regardless of test variables. The scotopic contrast hue has thus been assumed to be controlled basically by the disposition produced by chromatic stimulation of cones. In conformity with the suggestion, the scotopic hue has been found to be broadly invariant of wavelength and intensity of test-stimulation (STABELLand STABELL, 1971b, 1972d). The question remains, however, whether it is bleaching or light signals from cones that cause the change in sensitivity of the opponent cells. At present, evidence seems to favour the second alternative (STABELL,B., 1968; STABELLand STABELL,1971~). It has been shown, for example, that scotopic hue may remain visible for more than one hour while cone pigments are thought to regenerate within a few minutes (cf. RUSHTON,1957). CONCLUSION There appears to be well-founded evidence in favour of the assumption that scotopic contrast hue originates centrally to the photochemical systems of the receptors, and results from interaction between cone and rod activities. Selective chromatic stimulation of the three types of cones is assumed to change the relative sensitivity of the opponent cells, producing a disposition for scotopic hue which is triggered upon test-stimulation of rods. Rods may thus be thought to mediate every hue of the spectrum depending on the disposisition of the opponent cells. The achromatic aspect of night vision is observed only under conditions where the opponent cells are in a neutral state. In opposition to Helmholtz’s color theory (HELMHOLTZ, 1896) it is thus suggested that receptors that are morphologically and biochemically identical may give rise to different sensations of hue. REFERENCES ABRAMOV, I. (1968).Further analysis of the responses of LGN cells. J. opt. SOC.Am. S&574-579. ALPERN, M. (1965).Rod-cone independencein the after-flasheffect. J. Physiol., Land. 176,462-472. AUBERT,H. (1865) Physiologic der Netzhaut. Morgenstern, Breslau.
BROWN,J. L., METZ,J. W. and YOHMAN,J. R. (1969). Test of scotopic suppression of the photopic process. J. opt. Sot. Am. 59, 1677-1678. BROWN, K. T. and MURAKAMI, M. (1968). Rapid effects of light and dark adaptation upon the receptive field organization of S-potentials and late receptor potentials. Vision Res. 8, 1145-1171. BROWN, P. K. and WALD, G. (1964). Visual pigments in single rods and cones of the human retina. Science, N. Y. 144,45-52. DE VALOI~,R. L., ABRAMOV, I. and JACOBS,G. H. (1966). Analysis of response patterns of LGN cells. J. opr. Sot. Am. 56,966-977. DODT, E. and JESSEN,K. H. (1960). Depression of cone sensitivity during dark-adaptation. Experientiu 16, 205-206. EBBINGHAUS, H. (1893). Theorie des Farbensehens. 2. Psychol. Physiof. Sinnesorg. 5, 145-238.
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FFXJM~_ T. E., SEKULFX,M. D, and Russ, E. H. (1972). Rod-cone interaction in human scotopic vision. Science, N. Y. 175,913-914. GOURAS,P. and LMK, K. (1966). Rod and cone interaction in dark-adapted monkey ganglioncells. f, Physiat.,
Land. l&$,499-510.
GRAN~T, R. (1963). Sensory &fechanismsof the Retina. Hafner, New York. HECHT, S. (1937). Rods, cones, and the chemical basis of vision. pi~J~+riol. Ret>. 17, 239-290. HELMHOLTZ,H. VON (1896). Handbuch der physiologischen Optik. Leopold Voss, Hamburg and Leipzig. HERING, E. (1878). Zur Lehre cum Lkhtsinne. Carl Gerold Sohn’s, Wien. HERING,E. (1964). Ouflines ofa jrbeory ofthe Light Sense (Translated by L. M. HURVICHand D. JAMESON), Harvard Univ. Press, Cambridge, Mass. IKEDA, M. and URAKUBO,M. (1969). Rod-cone interrelation. J. opt, Sot. Am. 59, 217-222. K.ONIG,A. (1894). uher den menschhchen Sehpurpur und seine Bedeutung fiir das Sehen. SirrBer. Pt-euss. Akad. Wk. 2, Halbhd., 577-598. LIE,I,(1963). Dark adaptation and the photochromatic interval Docunrenia ophth. 17,41 t-510. L~TH~OE, R. f. (1940). The mechanism of dark adaptation. A critical resumg. Br, .K Uphth~~~ 24,21-43, MARKS, W. B., Dom~~x+ W. H. and MacNr~o~~ E. F. (1964). Visual pigments of singIe primate cones. Science, N.Y. 143,1181-1182. Mrr~linr, G., S~AFTIC~N, G., VALLECALLE, E.,FATEHCHAND,R., VUEGAS, J. and LAUFER,M. (1961). Glianeuron interaction and adaptational mechanisms of the retina. In Neurophysiofogieund Psychophysik des visueilen Systems (edited by R. JUNG and H. KORNHUBER),pp. 463-481, Springer, Berlin. PURKINIE,J. (1825). Beobachtuttgen und Versuche zur Physiologic der Sinne. Neue Beitriige _wr Kenntniss des Sehens in subjectiver Hindsicht. Vol. 2. Reimer, Berlin. RUSHTON,W. A. H. (1957). Physical measurements of cone pigment in the living human eye. Nature, Land. 179,571-573. RUSHTON,W. A. H. (1965). The Ferrier Lecture: visual adaptation PKJC. R. Sot., B. 162, 20-46. STABELL,B. (1967). Rods as color receptors in scotopic vision. Scud. J. Psycho!. 8, 132-138. STABELL,B. (1968). Rod vision as chromatic vision. Scund. J. Psycho!. 9, 282-288. STABE~L,B. (1969). Transition from rod to cone vision. I. Simultaneous contrast. Seand. J. Psychol. IO,
61-644. STABELL, B. and STABELL, U. (1967a). Night vision as chromatic vision. Stand J. Psucfraf. 8,145-149.
STMW_L,B. and STABELL,IJ. (1967b). Color threshold ~~ure~~ts
in scotopic vision I. Pre-stimulation varied. SCQZXZ.T. Psychol. 8,268-272. STA~)ELL,B. and STABU~, IJ. (1969a). Transition from rod to cone vision. II. Successive contrast. Semd. J.
Psychol. l&137-139. STABELL,3. and STABELL,W. (1969b). Chromatic rod and cone activities as a function of the photochromatic interval. Scund. J. Psycho/. 10, 215-219. STABELL,B. and STABELL,IJ. (1971a). Facilitation of chromatic cone activity by rod activity. I. Red-related cone activity. Stand. J. Psychal. If, 99-105. STABELL, B. and STABELL, W. (197lb). Chromatic rod vision I. Wavelength of test-stimulation varied. Stand. J. Psychol. 12, 175-178. STABELL,B. and STABELL,U. (1972a). Chromatic rod vision. III. Duration of pro-stimulation varied. Scann! J. Psychof. 13, 136-140. STABELL,B. and STABELL,W. (1972b). Chromatic rod vision. IV. Time between pre- and test-stimulation varied. Scatuf. J. Psychol. 13,141-W. ST~BELL, 8. and STABELL, Il. (1973a). Chromatic rod vision. VII. Intensity of pre-stimulation varied. Stand. J. PsychoA 14. STABELL, W. fl967f. Rods as color receptors in photopic vision Stand. J. Psycho{. % 139-144. STA~ELL, U. and STABEJ_L, B. (1965). Rods as color receptors. Stand, f. Psycfiof. 6, 195-260. STABELL,U. and STABELL,B. (1968a). Color threshold measurements in scotopic vision. II. Test-stimulation varied. Stand. J. Ps~+chol. 9,129-132. STABELL,U. and STABELL,B. (1968b). Color threshold measurements in scotopic vision. III. Simultaneous color contrast. Scond. J. Psychok 9, 133-137. STABELL,U. and STABELL,B. (1969c). Transition from rod to cone vision. III. Successive contrast anew.
Stand. J. Psycho/. 10,140-144.
STABELL,IJ. and STABELL,B. (1971c). Duration of scotopic contrast hue. Stand. J. Psychol. 12, 106-112. STABELL,U. and STABELL,B, (1971d). Facilitation of chromatic cone activity by rod activity. II. Variation of chromatic-related cone activity, Scund. S. Psychol. 12, 168-174. STABELL, U. and STABELL, B. (197le). Chromatic rod vision. II. Wavelength of pre-stimulation varied.
Stand. J. Psychof. 12,282~288. STABELL,W. and STABELL, B. (1972~). Chromatic rod vision. V. Retinal location of stimulation varied. Sfnltb. J. P&WA 13. STAEELL, U. andSTABELL,B. (1972df. Chromatic rod vision. Vf, Intensity of Tut-stimulation varied. Stand, J. Psyckoi. 13.
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Rod Vision-IX.
A Theoretical Survey
45.5
U. and STABELL,B. (1973b). Chromatic rod vision. VIII: Simultaneous contrast. &and. J. P&rol. 14. WALD, G. (1964). The receptors of human color vision. Science, N. Y. 145, 1007-1017. WALD, G. (1967). Blue-blindness in the normal fovea. J. opt. Sot. Am. 57, 1289-1301. WALD, G. and BROWN, P. K. (1958). Human rhodopsin. Science, N. Y. 127,222-226. WESTHEIMER, G. (1970). Rod-cone independence for sensitizing interaction in the human retina. J. Physiol., Land. 206, 109-116. WIESEL,T. N. and HUBEL,D. H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J. Neurophysiol. 29, 1115-l 156. WILLMER,E. N. (1946). Retinal Structure and Colour Vision. Cambridge University Press, Cambridge. WILLMER.E. N. (1949). Low threshold rods and the vercevtion of blue. J. Physiol., Lmd. 11. 17P. WILLMER;E. N. ‘(1965). Duality in the retina. In Cilour -Vision: Physiology-and kxperime&l PsychoIogy (edited by A. V. S. DE REUCK and J. KNIGHT), pp. 89-109. Churchill, London. STABELL,
Abstract-Theories of rods as color receptors are reviewed and evaluated. There appears to be well-founded evidence in favour of the hypothesis that rods and cones may interact to produce sensation of hue. Accordingly it is suggested that light signals from cones may change the relative sensitivity of the spectrally opponent cells, producing a disposition for scotopic hue that is triggered upon test-stimulation of rods. R&sumt!-On passe en revue et on discute les theories qui confient aux bltonnets un role dans la reception coloree. Des arguments sdrieux semblent en faveur de l’hypoth&se dune interaction des batonnets et des cones pour produire la sensation de tonalitd. On suggere done que les signaux lumineux des cbnes peuvent changer la sensibilite relative des cellules spectralement antagonistes, ce qui permet une tonalitd scotopique par stimulation des batonnets. Zusammenfasstmg-Theorien, die Stabchen als Farbrezeptoren betrachten, wurden iiberpriift und abgeschatzt. Es scheinen wohlbegriindete Anhaltspunkte dafiir zu sprechen da8 Stgbchen und Zapfen bei der Farbempfindung zusammenwirken. Dementsprechend wird vermutet, daD lichterregte Zapfen die relative Emptindlichkeit der spektral entgegengesetzten Zellen verandern konnen, indem sie die Farbemptindung im skotopischen Bereich so voreinstellen, da6 sie durch einen Testreiz der Stabchen au&&t wird.
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