Visual sensitivity and color vision in ground squirrels

Vision Res.

Vol. 11,pp. 51l-537. Pergamon Press1971.Printedin GreatBritain.

VISUAL

SENSITIVITY AND COLOR IN GROUND SQUIRRELS GERALD

VISION

H. JACOBS and ROBERT L. YOLTON

Department of Psychology, University of California, Santa Barbara, Calif. 93106,

U.S.A.

(Received 12 August 1970) INTRODUCTION ANIMALS from the family Sciuridae are of considerable interest to those concerned with the study of vision and visual systems. Within this family there is an unusually wide variation in visual structure and visual behavior, ranging from all-rod to all-cone retinas, and from strongly nocturnal to strongly diurnal visual behavior (WALLS, 1941). Among the species in this group, the ground squirrels have been a particularly intriguing target for experimentation and, as a result, a variety of kinds of information which bear on vision in these animals have been obtained. All of the species of ground squirrels that have been examined to date are reported to possess only cone receptors (VILTER,1954; TANSLEY, 1961; VAIDYA, 1964; DOWLING, 1964). The retinas of these ground squirrels are also typical of the prototype all-cone system in that the receptor to ganglion cell ratio is relatively low (VILTER, 1954). There is no urea centralis evident in these retinas although some other regional specializations may exist (VAIDYA, 1964). A variety of electroretinographic (ERG) measures made on ground squirrels also support the conclusion that the retina contains only cone receptors: (a) the ERG of the ground squirrel shows prominently the positive off-response associated with cone activity (TANSLEY,COPENHAVER and GUNKEL, 1961a, 1961b); (b) the ERG of the ground squirrel has the high fusion-frequency characteristic of cone activity (TANSLEY, 1961); (c) ERG recovery in the dark following light adaptation is rapid in the ground squirrel and occurs over a relatively restricted range of sensitivity, with a subsequent threshold some 1000 times higher than that of the all-rod rat (BORNSCHEIN, 1954; DOWLING, 1964). Thus, the available anatomical and electroretinographic data indicates that vision in the ground squirrel is based on the operation of only one class of retinal receptorscones. The nature of the retinal photopigments of the ground squirrel is unclear. DOWLING (1964) reported that only a single photopigment (having maximal absorption at 523 nm) could be detected by microspectrophotometric measurements on the retina of the 13-line ground squirrel. Subsequently, however, it was revealed that, “the high concentration of cytochromes in the retina prevented reliable absorption measurements at wavelengths shorter than 480-490 nm” (MICHAEL, 1968), and thus a second photopigment with major absorption in the short wavelengths could have gone undetected. Indeed, there is some indirect evidence to suggest the occurrence of multiple photopigments in the groundsquirrel retina. Measurements of spectral sensitivity have been made by means of the ERG on several species of ground squirrels (TANSLEY et al., 1961b; ARDEN and TANSLEY,1955; CRESCITELLI and POLLACK,1966). Sensitivity functions determined in this way have sometimes been found to show multiple sensitivity peaks, and shifts in relative spectral sensitivity 511

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in response to chromatic adaptation-both of these phenomena are often taken as evidence that more than one retinal photopigment is operative. Recently, MICHAEL (1968) has reported, on the basis of single-unit recording, that some of the optic-tract fibers in the ground squirrel yield chromatic-opponent response patterns. This latter finding is also taken to indicate the occurrence of two or more photopigments. In spite of the remaining uncertainties about the retinal photopigments, the strongly diurnal behavior exhibited by ground squirrels has naturally led to questions about the possibility of color vision in these animals. In an early study, KOLOSVARY (1934) demonstrated the occurrence of pronounced color preferences in the souslik (Citelltls citellus). This result does not, however, yield any critical information on color vision in this species since no attempt was made to account for brightness. More recently, BONAVENTURE (1959) has searched for color vision in this same species. He first obtained measures of the spectral luminosity function for this squirrel and used these results to control brightness cues in subsequent wavelength-discrimination tests. The result of these latter tests was that the ground-squirrel subjects were eventually able to discriminate between a variety of pairs of spectral stimuli when brightness was controlled, and Bonaventure concluded that this species possesses a “good color vision”. It might be noted that the luminosity function obtained in Bonaventure’s study (which served as the basis for brightness control) is quite unlike any of the other estimates of spectral sensitivity for ground squirrels. CRESC~LLI and POLLACK(1965, 1966) have obtained positive evidence for color vision in the antelope ground squirrel (Citellus leunrrur). They found this squirrel was able to successfully discriminate between several pairs of spectral stimuli when brightness cues were eliminated, or made irrelevant, by using sensitivity estimates obtained from the ERG, and by wide variations in stimulus luminance. Both of these latter behavioral studies, therefore, suggest that at least some species of ground squirrels do possess some degree of color vision. There are several motivations for studying vision and the visual system in ground squirrels. For purposes of furthering our understanding of all-cone visual systems, for providing the psychophysical bases for behavioral-physiological comparisons, and for adding information that might bear on the questions associated with understanding the evolution of color vision systems, it would be useful to have a detailed inventory of the visual capacities of the ground squirrel. To provide such information, a series of experiments directed toward assessing several features of visual sensitivity and color vision have been completed on animals representing two species of ground squirrels. METHOD Subjects. The subjects were 134ine ground squirrels (CitelJns tr -tu) and Mexican ground squirrels (Citdlus ~)(Howar,1938).Thefonmsr~mppedinths~olDssrfbld,Illinois, U.S.A., the latter in Austin, Texas, U.S.A. All animals m adults and both sexa w rapcaented. Psycbophysical measurewnb were obtained from a total of 26 animals; 17 of this group compkted one or more problems and these are the animals which provided the twtdb presented here. Apparoluc. Au the probkms were set in the context of a thr&altemative -on task. The test cJumberutiIizedhadinterior~nsof23 x 31 x 33cm.AlongonewallofthischamberWethme circukr (dia. 3 cm) stimulus windows. which were made from ditiusing @ass and mounted in a horizontal line 6.5 cm apart. Mountal directly above each window was a response km and below each window was a cup into which food r&forcements delivexed. A fluoman t lamp was mountaJ in the roof of the chamber. In meet of the cxpc&nmb rqwtai horn this light was used to provide cimtinuous chamber liiting with a aman illuminaoce of 108 lmlm’. The chamber also contained a wau+muntedspcaker. The stimulus windows were trauGlluminated from outside of the test chamber. Three tungsten-f&unent projectors (150 W) were mounted so that each illuminated one of the windows (the maximum window

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luminance available from these sources was 136 cd/m’). The characteristics of the light illuminating each window was controlled through the use of Kodak Wratten step filters. In addition, any one of the windows could be illuminated with the output from a Bausch & Lomb monochromator (tungsten-iodide source) which was mounted on a turntable. Light from this source could either be added to, or could replace, the output from any one of the filament projectors. The slits of the monochromator were adjusted so as to yield a chromatic light having a half-energy passband of 10 nm (maximum window luminance at 550 nm = 14.3 cd/m’). Accessory shutters and timing gear were arranged to provide a variety of possibilities for presentation of stimuli and sequencing of events. Procedure. The animals were initially trained to select the stimulus window which appeared different from the other two windows when the basis for the difference was spectral content and/or intensity. The ground squirrels indicated their choice by pressing the lever mounted directly above the appropriate window, and most were able to learn this task readily. The appropriate control observations indicated that cues other than those under experimental control were successfully eliminated from the situation. Two reinforcement techniques were employed. Some of the animals were run under a 23-hr fooddeprivation schedule and received a 97 mg Noyes food pellet for each correct response. Other animals received intracranial stimulation as reinforcement. These animals were implanted with bipolar electrodes in the region of the posterior hypothalamus. Stimulus current level was initially adjusted for each of these animals in a free-response situation so as to produce a high rate of bar pressing. The current levels ranged between 35 and 150 pA. In the test situation, the implanted animals received a 250-msec, 60-Hz sinusoidal stimulation for each correct response. No systematic differences in discrimination performance were found between animals run under the two different reinforcement procedures. The procedures specific to each experiment will be detailed below. General features included the follow-

ing. Correction procedures were employed during training sessionsfor all of the discriminationproblems, whereasno correction was allowed during test sessions. Specific stimulus conditions were run in five-trial blocks. The position of the positive stimulus was randomized among the stimulus windows with the restriction that each of the three windows was positive an equal number of times in each test session. Foodreinforced animals received an average of 100 trials per daily session, while animals run for brain stimulation completed an average of 300 trials per session.

A. Visual Sensitivity For the purposes mentioned above, several features of visual sensitivity in the ground squirrel must be known. The following basic indices of visual sensitivity were therefore determined: (a) the form and variability in the spectral sensitivity function, (b) spectral sensitivity functions under several levels of achromatic adaptation, (c) the course of sensitivity change during recovery from light adaptation and, (d) the effects of chromatic adaptation on spectral sensitivity. 1. Spectral sensitivity Detailed measurements of the spectral sensitivity function are required for useful comparison to photopigment measurements and to electrophysiological indices, and as a pre-requisite for the various tests of color vision. Accordingly, a large number of measurements were made to provide a reliable indication of the spectral luminosity function for the ground squirrel. Procedure. Luminosity functions were determined by using an increment-threshold procedure; monochromatic light was added to an achromatic background at multiple test wavelengths and the intensity of the monochromatic light required for some criterion level of discrimination was determined. On a given trial, a shutter was opened so that all three stimulus windows were illuminated, two of them with achromatic light and the third (the positive window) with the same achromatic light plus the output from the monochromator. The animals were trained to select the positive window quickly so that the trial duration did not exceed 5 sec. When the animal responded, reinforcement was automatically delivered if a correct choice had occurred and all stimulus lights were occluded by shutter closure. Each animal was initially trained on an easy discrimination, i.e. with a high-intensity monochromatic light added to the background and with stimulus wavelength set in the range from 500 to 540 nm. When the animal was performing this task with a high degree of accuracy, the intensity of the monochromatic light was systematically reduced so that, eventually, a range of stimulus intensities was determined such that the animal’s performance went from chance to near-perfect discrimination.

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For the determination of the spectral huninosity function, the following conditions were used. The background light was filtered to yield a window luminance of 0.14 cd/ml. Sensitivity was determined for 11 test wavelengths taken at 20 MI intervals from 440 to 640 run. The intensity of the monochromatic light was varied in steps of 0.3 log,, units and the order of intensities tested was random within a test session. Only a single wavelength was tested within a session. A minimum of 100 observations was accumulated at each stimulus intensity-wavelength combination for each animal, although frequently many more were obtained. Following the initial test wavelength which was always in the 500-540 MI range, the order in which the different wavelengths were tested was randomized across subjects. The total number of test trials required to adequately detine the luminosity function varied rather widely from animal to animal, from ca. 5000 to 14,000. Since it required several weeks to determine the entire function, several of the animals were retested on some of the stimulus wavelengths to assure that no progressive changes in behavior had occurred; none were found. Eight ground squirrels, five C. mexicanus and three C. tridecemlineatus, completed this problem. Both reinforcement techniques and both sexes were represented for each species.

Results Psychometric functions were derived for each animal at all of the test wavelengths. Figure 1 shows the mean psychometric functions for five Mexican ground squirrels. As can be seen, performance fell off smoothly as the intensity of the added monochromatic light was decreased-straight lines have been drawn through the data points in this figure to show the nearly linear relationship between discrimmation performance and log stimulus intensity over the range from about 40 per cent to 80 per cent correct. Psychometric functions for the individual subjects were similar in nature to those shown in Fig, 1. Spectral luminosity functions for each of the animals were obtained from psychometric functions of the type shown in Fig. 1. The criterion discrimination level used for this purpose was 50 per cent correct but, as can be inferred from the results shown in Fig. 1, there would be essentially no differences in the shapes of the derived functions for any criterion level between 40 per cent and 80 per cent correct. The spectral luminosity functions obtained from the base of an equal-energy spectrum are given in Fig. 2 where the mean sensitivities

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1. Psychometric functions obtained from Mexican ground squirrels on the spectral sensitivity test. Each plotted point represents the mean discrimination performance of five animals. Functions for the individual wav&ngths have been shi laterally for clarity. Each horizontal scale division corresponds to one log r0 unit of intensity. Chance performance is 33 per cent correct.

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FIG. 2. Spectral luminosity functions for five Mexican and three 13-line ground squirrels. The plotted points are mean sensitivityvalues for each group. The vertical lines enclose the total range of sensitivityfor all squirrels at each test wavelength.

and the total range in sensitivity at each test wavelength is shown separately for Mexican and 13-line ground squirrels. The range in sensitivity is quite small among the animals tested and, further, both the absolute sensitivity levels and the form of the spectral luminosity function appear similar for the two species. Indeed, there were no statistically significant differences in sensitivity between subjects or between species. Since the results for the eight squirrels tested were not significantly different, the functions were combined. The mean spectral luminosity function so obtained is graphed in Fig. 3. The luminosity function for the ground squirrel, under the conditions of measurement employed here, is simple in form with a single sensitivity maximum at about 520 nm and an absence of submaxima. The fall-off in sensitivity at the long wavelengths is particularly striking, with sensitivity to 640 nm some two log,, units down from peak sensitivity. 2. Spectral sensitivity and adaptation state In order to determine if there are systematic changes in spectral sensitivity as a function of the adaptation state, and to measure the magnitude of the sensitivity change caused by a change from the light-adapted to the dark-adapted state, spectral luminosity functions were measured on ground squirrels for several combinations of background and ambient light. Procedure. Complete spectral luminosity functions were determined under four different adaptation conditions using the methods, numbers of observations, and criteria described for the previous experiment. For three of these conditions, the usual ambient light (10.8 lm/m*) was present in the test chamber but the background light level was varied so that sensitivity determinations were obtained for background levels of 0*14,0$ and 1.4 cd/m2. In the fourth condition the light in the test chamber was turned off and the monochromatic light appeared on a zero background. Two Mexican ground squirrels served as subjects.

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GERALD H. JACOBSAND ROBERTL. YOLTON

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function for eight ground squitrcls.

Results Luminosity functions derived for the two ground squirrels under the four conditions of adaptation are shown in Fig. 4. Absolute sensitivity diffbrenccs are re&ted in these plotted functions and, as can be seen, the range of sensitivity change and the mean sensitivity for each adaptation state is about the same for both subjacts. Peak sensitivity occurs in the vicinity of 520 nm for both subjects at all states of adaptation. In addition to maintaining the same spectral peak, the shapes of the luminosity functions are all approximately the same except for those functions obtained on the highest background level. For this latter condition, peak sensitivity remained at about 520 nm for both animals but some inhomogeneities appeared in the functions-most obviously, a notch appears at about 480 MI. Another important feature of the results presented in Fig. 4 is the total range of sensitivity. The top two curves in that figure represent spectral sensitivity under low-level light adaptation and for the dark-adapted condition. The absolute difference in sensitivity for these two states amounts to slightly more than one log unit. A human subject tested under these same conditions showed a sensitivity change of about three log units, coincident with a shift from photopic to scotopic sensitivity. Thus, the dynamic sensitivity range for the ground squirrel, as measured in this fashion, is relatively small. The results of this experiment suggest that the same retinal photopigments probably underlie spectral sensitivity in the ground squirrel under both light and dark-adaptation conditions: there is no evidence for any change cormsponding to a Purkinje shift. However, the fact that there are some discriminowe changes in the shapes of the functions as a result of adaptation change implies that more than one retinal photopigment may contribute to the luminosity function.

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Visual Sensitivity and Color Vision in Ground Squirrels

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FIG. 4. Spectral luminosity functions for two ground squirrels under four different conditions of adaptation. See the text for details.

3. Dark adaptation

The previous experiment provided some indication of the extent of the sensitivity change for the ground squirrel between dark-adapted and light-adapted conditions. In that experiment it was difficult to control adaptation state precisely; for example, it is unlikely that in the dark-adapted condition the animals had achieved maximal sensitivity. A more controllable, and traditional, means to assess this change in sensitivity is to determine directly the dark-adaptation function. This procedure has the virtue of providing information about the time course of sensitivity change, as well as an indication of the final level of sensitivity achieved. Procedure. Dark adaptation was measured in the same three-alternative situation used for the other problems. The squirrels were initially trained to respond during the occurrence of a NO-Hz tone which was presented for 2 sec. After they had learned to reliably select the illuminated window during the tone period, dark-adaptation measurements were made. For the dark-adaptation measurements presented here, the following conditions were employed. Animals initially received 10 min of dark adaptation at the beginning of each test session, then 5 min of exposure to the illuminated test chamber (average illuminance of 29.1 lm/m*). At the end of the light adaptation period the light was extinguished and then stimulus presentations followed at 6-set intervals through the course. of dark adaptation. At the end of each run the animal was reexposed to the light for a 2-min period before another dark-adaptation sequence was initiated. After the total range of sensitivity change had been established, the dependent measure utilized was the minimal time into the dark-adaptation period required for three successive correct choices of the positive window at a given stimulus intensity. This entire sensitivity range was investigated in each test session. The test wavelength used for all of these measurements was 550 nm. One of the advantages of using intracranial stimulation as a reinforcer is that “consummatory” time can be both brief and controlled, two features necessary for the measurement of time-dependent processes. Thus, the subjects in this experiment, one Mexican and one 13-line ground squirrel, were run with intracranial stimulation as the reinforcement. A single human subject was run under exactly the same stimulus conditions and forced-choice procedures as the squirrels except that the human observer viewed the window display from a distance of 36 cm.

GERALD H. JACOBSAND ROBERTL.

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Results The subjects were run on the procedure described above for a period of severa weeks, until measured t~esholds showed no further systematic changes. Following this training period, 20 additional determinations of the dark-adaptation function were made. The means of these latter values are plotted in Fig. 5 for both the ground squirrels and the human observer. As can be seen in Fig. 5, the data obtained from the two ground squirrels corresponded closely, both in measured sensitivity and in the time course of recovery. The dark-adaptation functions for these animals have the familiar exponential form and there is no strong indication that more than one recovery process is operative, i.e. there are no clear breaks in the curves, although the function for one animal does show the hint of a discontinuity at about 100 set into dark adaptation. The total change in threshold for the ground squirrel,

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FIG. 5. Dark-adaptation curves for two ground squirrels and one human observer. Each plotted point represents the mean of 20 separate determinations. The curves for the human and the squirrets have been shifted vertically to squata their respective senaitivitics at the end of light adaptation. The human thresholds WCcquaf to the ordinate vabs multiplied by i-4 cd/m’. The horizontal line at the upper left shows the approximate cone threshold level for the human obsu~er.

following moderate light adaptation, is somewhat less than two log,, units-this figure is slightly larger than the change in sensitivity observed in the previous experiment where spectral lu~nosity functions were obtained under dark and light adaptation. We were unable to find any significant increase in sensitivity after about IO min of dark adaptation. Comparison of the results obtained from the human observer and those from the squirrels, as shown in Fig. 5, yields a number of intoresting conclusions. For the rather low level of light adaptation achieved in this experiment, the recovery function for the human observer is one that is characteristic of rod activity. Sensitivity was measured for both squirrels and humans at increment threshold in the li#G4apted state and the differences found in this comparison were used to correct the data in Fig. 5 so that the absolute differences in threshold shown thcrc are an accurate reflection of tho differences in sensitivity of man and ground squirrel during dark adaptation. After about 10 min of adaptation the rod

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threshold for the human is some 3.5 log,, units lower than the corresponding threshold for the all-cone ground squirrel. An estimate of the cone threshold for the human subject in this test situation is indicated by the horizontal line at the left of Fig. 5. It is apparent from this latter measurement that the maximal cone sensitivity for man is not greatly different from the measured maximal sensitivity for the ground squirrel. 4. Effects of chromatic adaptation on spectral sensitivity The form of the spectral luminosity function for the ground squirrel, at least under some conditions of measurement, suggests the occurrence of more than one underlying mechanism. If more than one photopigment exists in this retina, it ought to be possible through chromatic adaptation to differentially alter the shape of the luminosity function, The experiment reported here was designed to test this possibility.

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FIG. 6. Spectral luminosity functions for one ground squirrel determined on both neutral and chromatic backgrounds. The solid line shows spectral sensitivity for the neutral background, the broken line for the chromatic background. The dominant wavelength of the chromatic background is indicated by the vertical arrow. Procedure. Spectral luminosity functions were obtained from one 13-line and one Mexican ground squirrel on both achromatic and chromatic backgrounds following the methods outlined in Experiment 1. In addition, these animals were initially trained to respond during the presentation of a tone in the same manner as described for the subjects in Experiment 3. The test light then appeared as a 2-set flash added to the relevant background light which was on continuously. The intertrial interval was 10 see. The effects on the luminosity function of two different chromatic backgrounds were explored in some detail. These chromatic backgrounds were produced by inserting Kodak Wratten color filters (No. 29 with dominant wavelength of 633 nm, and No. 98 with dominant wavelength of 452 nm) into the beams of the projectors. Complete luminosity functions were obtained at several intensity levels for both of these background conditions.

Results The results of these chromatic-adaptation procedures yield a straightforward answer to the experimental question. This outcome is illustrated in Fig. 6 which shows the spectral

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luminosity functions for one squirrel obtained with an achromatic and with a chromatic background. For that background light (produced through the Wratten No. 98 filter) there is no change in sensitivity at the peak of the luminosity function (520 nm). In the spectral region of the background light, however, there is a substantial loss in sensitivity which, in general, becomes progressively smaller as the test wavelength departs from the dominant wavelength of the background light. The chromatic background utilized to generate the data for Fig. 6 also produces a noticeable sensitivity enhancement at about 560 nm. The other chromatic backgrounds investigated produced the same kinds of changes in the luminosity function, although frequently much more complex in nature. The results of this experiment indicate clearly that the ground-squirrel retina must contain two (or more) photopigments which respond differentially to chromatic adaptation. Discussion The results from the four experiments on visual sensitivity provide the basis for a consideration of some relationships between visual sensitivity and results from investigations of retinal anatomy, photopigments, and electrophysiology for the ground squirrel. Characteristics of the spectral sensitivity function As detailed in the Introduction, there is no anatomical evidence to sugge& the occurrence of other than cone receptors in the ground squirrel retina, and a variety of electrophysiological results support this observation. The results from the experiments reported here add behavioral evidence to support the view that the only operative photoreceptors in these squirrels are cones. The most important such evidence is: (a) that there is no shift in the spectral location of maximal sensitivity as a function of adaptation state and, (b) that the dynamic range of sensitivity is rather restricted, as is cone sensitivity in other species. In view of this latter result, a report by LINSDALE(1946) from a field study of C. beecheyi is of interest. He noted that, “squirrels do not see well in dim light”; Fig. 5 of this study documents empirically this lack of sensitivity to low light levels. It should also be recalled in this connection that estimates of maximal sensitivity for the ground squirrel and maximal cone sensitivity for human subjects are quite similar despite the large number of other differences in their respective visual capabilities. Peak spectral sensitivity for the eight ground squirrels tested was at 520 nm; this figure is in reasonable agreement with estimates.obtained in several other studies in which the ERG was used as a criterion measure (ARDENand TANSLBY,1955; TANSLJZYet al., 196lb; CRESXELLI and POLLACK,1966). In addition to these measures, PAK and EBREY(1966) reported maximal sensitivity of the early receptor potential of the ground squirrel retina to be at 540 nm, although only a few spectral points were tested. The results most discrepant from the present ones are those reported by BONAVENTURE(1959) for the souslik. Spectral sensitivity in this latter (behavioral) study was found to be maximal at 555 nm, a location rather removed from all of the other estimates for the ground squirrels and, in particular, quite different from the ERG measurements made by ARDENand TA~LEY (1955) on the same species. The spectral sensitivity function for the ground squirrel is simple in form under the conditions of testing utilized here. Evidence was obtained for the presence of more than a single underlying mechanism from the findings that: (a) a more complex sensitivity function could be obtained by increasing the luminance of the background light and, (b) the shape of the function could be distorted by measurement on a chromatic background. Most of

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the previous investigators of spectral sensitivity in ground squirrels have found secondary peaks in the sensitivity function: in the region of 470-480 nm by ARDENand TANSLEY(1955) and CRESCITELLI and POLLACK(1966) and at 502 nm by TANSLEYet al. (1961 b). The presence of secondary peaks in these ERG studies reinforce the conclusion from our findings that more than one operative mechanism contributes to the spectral sensitivity function. The appearance and character of the complexity in the resulting spectral sensitivity function presumably depends, among other things, on the stimulus conditions employed, e.g. state of adaptation, etc. Photopigments and spectral sensitivity

The literature provides some information about the nature of the photopigments in the ground squirrel retina. DOWLING(1964) measured directly a photopigment in the 13-line ground squirrel which had peak absorption at 523 nm. Later, MICHAEL(1968) reported that, as a result of chromatic-adaptation procedures, evidence for two spectral mechanisms could be obtained in the Mexican ground squirrel. One of these mechanisms had peak sensitivity at 520 nm, while the other showed maximal sensitivity in the region of 460 nm. Thus, the best estimate about the character of the photopigments in the ground squirrel retina is that there are only two, and that they have respective peak absorptions at about 460 and 520 nm. Due primarily to the observations and theories of WALLS(1931, 1940), the pronounced pigmentation that is characteristic of the lenses of the squirrels is well known. Indeed, a fresh lens obtained from the eye of a ground squirrel appears much yellower than a comparable lens taken from a primate eye. Any consideration of the relationship between the photopigments and spectral sensitivity in the ground squirrel must obviously take into account the pronounced selective filtering by the intraocular media. Measurements made by MICHAEL(1965) of the absorption characteristics of the lens and cornea in the Mexican ground squirrel are shown in Fig. 7, where the mean values for nine animals are given. Transmission characteristics for the lens and cornea in the antelope ground squirrel have also been reported and these do not differ greatly from the measurements shown in Fig. 7 (CRESCITELLIand POLLACK,1966). Figure 8 shows the mean spectral sensitivity function for the eight ground squirrels tested. This sensitivity function is corrected for the absorption by the intraocular media and it is calculated from the base of equal quantum intensity. The point at 420 nm shown in Fig. 8 is based on the results from only a single squirrel and it should not therefore be given the same validity as the other plotted points. The spectral sensitivity function, as measured at the retinal level for Mexican and 13-line ground squirrels, shows peak sensitivity at about 500 nm with a strong secondary peak at 460 nm. This sensitivity function shows general agreement to several of the functions obtained from the ERG studies which were mentioned above. The form of the corrected sensitivity function shown in Fig. 8 quite cIearly could not be produced through the direct operation of only a single retinal photopigment. Evidence that the sensitivity function could, however, be generated through the operation of the two presumptive photopigments can be evaluated from the information given in Fig. 8 where the absorption spectra for photopigments having peak absorptions at 460 and 520 nm, and shapes generated from the Dartnall nomogram (DARTNALL,1953), have been drawn in. It can be concluded from an examination of Fig. 8 that two photopigments showing peak absorptions at 460 and 520 nm are adequate to account for the spectral sensitivity of the

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ground squirrel. Finally it might be noted that, although no systematic attempt to do so has been made, an exact match between these presumptive photopigments and the spectral sensitivity function cannot be obtained by either a simple summation procedure or by assuming that only the most sensitive photopigment at any given spectral location controls sensitivity-some degree of inhibitory interaction between the two photopigments is apparently required. Electrophysiological results and spectral sensitivity In a series of experiments MICHAEL(1968) has examined the response characteristics of single optic nerve fibers in the Mexican ground squirrel. Among other features, these units show two basic spectral response patterns which are similar in form to those observed in

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numerous other species. One of these types of units reaponds with either an excitatory or an inhibitory change to all spectral stimuli, but the magnitude of this change is graded as a function of stimulus wavelu@h (nonopponent unit); the other type shows both excitatory and inhibitory change with the direction and ma@ude of the response a function of stimulus wavelength (chromakopponent unit). For primate visual systems some attempts have been made to relate the oprntion of such units to the visual functions they subserve (DE VAUXS and JACOBS,1968). SpocifkUy, in these correlative attempts, the opponent cells were assumed to transmit i&on&ion mainly useful for color vision while the nonopponent cells transmit information utilized for achromatic vision. It is of some interest to see if these same relationships might hold for the ground squirrel visual system.

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Figure 9 shows the spectral sensitivity for one of the non-opponent units recorded from the optic nerve of the Mexican ground squirrel (MICHAEL, 1965) and the spectral sensitivity function determined in these experiments. Although the correspondence between the physiological and the behavioral data is by no means exact, it is reasonably close, particularly in view of the variability to-be expected among the responses of individual neural units. Thus, there is at least suggestive evidence that the same sort of role previously found for the non-opponent units in the monkey visual system also holds for the ground squirrel. It should be pointed out that the sensitivity function for the non-opponent unit shown in Fig. 9 does not fit well the spectral sensitivity functions determined on the higher background light levels (described in Experiment 2) and it might be suggested that for the ground squirrel, as apparently for the macaque monkey (SPERLING, SIDLEY, DOCKENS and JOLLIFFE, 1968), the spectral sensitivity function determined under some conditions must be produced by information supplied through the chromatic-opponent systems.

, 420

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for the ground squirrels after correction FIG. 8. Mean spectral sensitivity function (-) for the absorption by the cornea and lens (Fig. 7). The broken lines show absorption functions for nomogram pigments having peak absorptions at 520 and 460 nm. The spectral sensitivity and the pigment curves have been equated at 520 and 460 nm.

B. Color Vision Comparative studies of animal color vision have been relatively few in number during the past few decades. In addition to the specific results, two general conclusions can be derived from a reading of this literature. First, the kinds of technical difficulties that plagued earlier studies, and consequently led to numerous disputes about the authenticity of results, are now widely recognized. In particular, the avoidance of brightness cues in presumptive color discriminations has become a clear requirement of any such experiment. The second conclusion from such research is certainly less widely publicized, but seems to be of equal importance. Tests of color vision on animal subjects are very time-consuming and thus such experiments that produce only a judgment as to whether or not an animal possesses color vision are, while interesting, not very useful and certainly are wasteful of experimental

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GERALD H. JACOBSAND ROBERTL. YOLTON

effort. Much more useful are investigations that yield, in addition to an indication as to whether or not an animal has color vision in the definitional sense, a variety of measures of that capacity, preferably measures that can be readily compared to information available from that most-studied of color-vision systems-man’s. As mentioned above, previous behavioral investigations of various species of ground squirrels indicate the presence of color vision. In addition, a variety of other evidence, including some presented here, suggest strongly that the minimal mechanisms required to produce color vision are present in Mexican and 134ine ground squirrels. Accordingly, several experiments were run to demonstrate the presence and ascertain some of the characteristics of color vision in these squirrels.

0

L

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t

I Wovelength,

nm

Fro. 9.chnpakon of the spectral hlmimxi ty function () and the spectral sensitivity m(____ ) for a non-opponent unit raxedcd from the optic tract of the ground squirrel.

1. Control of brightness cues In this section the procedures employed to insure that brightness cues were not available for the animal to use in the various tests of color vision are specified.

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in Ground

Squirrels

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Figure 10 illustrates, for one case, the results of the brightness matching procedure just described, In this instance the animal was required to djscriminate a monochromatic fight of 540 nm from two achromatic lights produced by inserting filters (Kodak Wratten No. 78M) into the beams of the projectors. Figure IO shows the fail-off in discrimination accuracy as the intensity of the monochromatic light was decreased. The equation points deter~~ed from two separate (and typical) runs are shown in Fig. IO. As can be seen, the two values so determined agreed closely, as in fact they did for other subjects so tested, Thus all brightness equations were achieved using both the information gathered from the luminosity tests and from direct subject matches. Finally, as will be noted where it is ~ppro~~ate, some additional variation in brightn~s around the equation values was systemati~a~l~~provided in each of the ~o~or-~sc~mi~at~o~ problems,

Lag UStenttUtion

FKL10.Intensity-responsefunctionsillustratingthe method used to obtain brightnessequation values for the tests of color vision on ground squirrels. See the text for details.

The ability of an animal to discriminate a chromatic from an achromatic stimulus, when stimulus brightness is not a differential cue, provides one defining condition for the presence of color vision. If, further, the character of the spectral stimulus is varied in such a task, some features of the color vision can be detailed. Thus, for human observers, the presence of a restricted xone in the visible spwtrnm&at cannot be d~~r~rnj~at~ from a white light (a neutral point) is considered to be diagnostic of d~chroma~y. Since both the presence and

GERALD H. JACOBS AND ROBERTL. YOLTOS

526

the location of such a neutral point can be readily investigated in the situation used for the previous tests on the ground squirrel, the neutral-point test provided a convenient first assay for color vision. Some of the data presented here were included in a preliminary report (JACOBS and YOLTON, 1969). Procedue. The same experimental situation that was used for all of the sensitivity determinations was employed for the neutral-point test, and for all of the other tests of color vision. In this test the negative stimuli were produced by filtering the output from the tungsten-lihunent projectors to produce a “white” light haying a color temperature of cu. 44WK and a hrminance of l-2 cd/m’. The positive stimulus was produced by the monochromator, with specika&ns.as described previously. The window iktminated with chromatic light and those ilhnninated with achromatic light were equated in brightness for the 4uirrel subjects by using the procedures described in the previous experiment. In addition, to be doubly certain that brightness was an irrelevant cue. the chromatic siimuli were prwened qua1 numkrs of times at the brightness-equation vahres and at values that were 03 log,, units more, or less, intense than the quation values. Subjects WNVJinitially trained to discriminate spactral lights set at 560 and 460 nm from the white and, atIer theee di&minations were mastered, the squirrels were tested at various points between 460 and 560 nm at intervals of 10.5 and 2.5 nm. Seven ground squirrels, four C. mexicanus and three C. fridxemheutus, completed this problem. 90

W-

40-

30 -

wowmgth,

nm

FIG. 11. Diaaimktion

perfomunca in the oautraf-poiat tat. Each plotted point IepfcsenIs twqxmaw for four Mexican and thxue 134iIlc gmmd 4uimls. thclm!an~ofThe vertial lines enclose the total range of performance at each test wav+agth. Results

All of the ground squirrels tested were able, after some training, to discriminate spectral stimuli set at 460 and 560 nm from white light. After the animals had acquired these initial discriminations, they were trained at spectral locations intermediate to these two points. The result of this procedure was that all of the subjects showed a loss of discriminative capacity in a zone extending from 500 to 510 am, but not elsewhere. As a consequence, this latter region was further examined in steps of 25 nm in the neutrai-point tests. Test runs involved various spectral stimuli from the range between 460 and 560 nm, presented in random sequence and at the intensities required for brightness equation with the variations described above. Usually only a few different wavelengths were tested in a

521

Visual Sensitivity and Color Vision in Ground Squirrels

single experimental session. Figure 11 shows the results of this test for both species. The data presented there are based on a total of 120 trials per spectral wavelength per animal. Several features deserve comment. First, as for the spectral sensitivity functions, there were no discemable differences in discrimination capacity between the two species of ground squirrels. Neither were there any differences in performance associated with the sex of the animal or the mode of reinforcement employed. Second, there were no systematic differences in discrimination across the three levels of stimulus intensity used. Figure 11 shows that all animals achieved 60 per cent correct discrimination or better for all test wavelengths, except those between 500 and 510 nm. In this region there was a sharp fall-off in discrimination accuracy and all animals performed at chance levels for the discrimination of 505 nm vs. white and, thus, all had a neutral point at this location,

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FE. 12. Discrimination performance in the neutral-point test with extended training. Three successive determinations are shown for one ground squirrel. Each plotted point represents the mean value for 60 test trials.

Previous studies of color vision on animal subjects have shown that individuals having severely anomalous, but not dichromatic, color vision may perform on initial neutralpoint tests so as to indicate the presence of a spectral neutral point (GRETHJZR, 1939; JACOBS, 1963). Such neutral points, seen in severely anomalous subjects, are evanescent and disappear with further training (JACOBS, 1963). Presumably this is because the cue that allows for discrimination in this region (the saturation difference between the white and the chromatic stimulus) is weak, but not absent. To be sure that the neutral points displayed in Fig. 11 were a true feature of the ground squirrel’s vision, some subjects were run through the neutral-point test several times. Figure 12 shows the results obtained from one such subject for multiple complete runs over the spectral range from 460 to 560 nm. The three determinations shown in this figure were each based on 60 trials per spectral point, and the determinations were separated by substantial numbers of training trials. It is clear that no

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YOLTON

significant changes in discrimination behavior occurred as a result of extended training, and therefore the neutral point recorded seems to be a real one. Although it seemed an unlikely prospect, some tests for a neutral point were also made outside of the spectral zone discussed above. In brief, no evidence was found for any loss of discrimination in any part of the spectrum from 450 nm to 590 nm except in the region of 505 nm. It will be noted that the highest levels of correct discrimination achieved in this problem were consistently lower than the highest levels reached in the various tests of visual sensitivity. Since all of the animals had large numbers of test and training trials in the neutralpoint situation, these differences are probably not attributable to any learning variable. Indeed, the asymptotic levels of performance for all of the problems where hue and/or saturation differences provided the basis for the discrimination were consistently lower than for those problems that could be solved on the basis of brightness differences. The results of this experiment lead to two conclusions. First, the fact that these animals were able to successfully discriminate spectral stimuli from white, in the absence of brightness cues, indicates that both Mexican and 13-line ground squirrels possess color vision. And second, the fact that they were unable to perform this discrimination over a restricted portion of the spectrum indicates the presence of a neutral point and, hence, dichromacy in these animals. Discussion The spectral neutral point was defined with some precision for these two species of ground squirrels; under these conditions of measurement it is clearly located between 502-5 and 507.5 nm. The amount of variability in spectral location for the seven animals tested corresponds quite well with the small variability seen in the locations of spectral neutral points measured on human deuteranopes and protanopes (W~tls and HEATH, 1956). Both the estimates of the characteristics of the photopigments in the ground squirrel, and the measurements of spectral sensitivity reported here suggest that the color vision of the ground squirrel might be expected to be similar to that of the human protanopic observer. However, the location of the spectral neutral point (505 nm) is displaced toward the long wavelengths relative to that generally reported for human protanopes (Prrr, 1935 ; HECHT and SHLAER,1936; WALLSand HEATH, 1956).* It is widely recognized that the location of the dichromatic neutral point is powerfully a&ted by the characteristics of the “white” light used for the test: most importantly, the lower the color temperature of the white light, the longer the wavelength at which the neutral Point is located. A second feature that could be expected to contribute to the neutral-point location is the heavy ocular pigmentation of these squirrels. Indeed, JUDD (1944) has made the suggestion that the heavier the degree of ocular pigmentation, the longer the wavelength at which the neutral point will be located. The obvious conclusion is that the spectral location of the neutral point should be understood in the context of the test-stimulus conditions, and of the possible contribution by pre-retinal filtering, rather than as some invariant feature of sensory capacity. For the dichromatic visual system, it might be expected that the spectral location of the crossover points for the chromatic-opponent cells in that visual system would correspond * This displacement is a feature of the ground-squirrel visual system since three human protanopes in the same apparatus showed normal neutral-point locations (mean location = 493 nm).

tested

Visual Sensitivity and Color Vision in Ground Squirrels

529

to the spectral location of the neutral point. Such crossover points for the units found in the Mexican ground squirrel are in the vicinity of 500 nm (MICHAEL, 1968)--this figure is not greatly different from that found here for the neutral point. 3. WaGelength discrimination By far the most common index of color vision is the capacity to discriminate between various spectral wavelengths. From the results of the previous experiment, and from information about wavelength discrimination in human dichromatic observers, these ground squirrels were expected to show good wavelength discrimination over only a relatively restricted portion of the spectrum. Results supporting this expectation are reported here. Procedure. Wavelength discrimination is usually measured by defining a standard wavelength and then determining how much different (in nm) a comparison wavelength must be in order to yield some criterion discrimination. In the situation used here, the standard stimulus appeared on two windows and the comparison stimulus was produced by the monochromator and appeared on the third window. As usual, the animal was reinforced for selecting that window which appeared different from the other two. Wavelength discrimination was measured around five spectral locations. These standard stimuli were produced by inserting Kodak Wratten filters into the beams of the projectors. The five filters used, and their dominant wavelengths, were as follows: No. 98(452 nm), No. 48(471 nm), No. 75(493 nm), No. 45 + No. 58(506 nm), and No. 74(538 nm). Pass-band characteristics for the monochromator were the same as for the previous experiments. Stimulus luminance for the monochromator set at 500 nm was 1.9 cd/m2 and all other stimuli, both standards and comparisons, were adjusted in intensity so as to be equal in brightness (for the ground squirrel) to this value by using the methods described previously. In addition to these equation values, a random variation in stimulus intensity amounting to i 0.2 log,, unit was employed. Animals were initially trained on either the No. 75 or No. 45 + No. 58 filters. The comparison stimulus was set at a value 30 nm or more away from the dominant wavelength of the standard. After the animal had mastered this discrimination, the comparison wavelength was shifted, in steps of 10 and 5 nm, toward the standard wavelength until discrimination performance dropped to chance levels. This procedure was repeated several times for approaches toward the standard wavelength from both spectral directions. Subsequently, wavelength discrimination was measured around the remaining four standard values. Two Mexican and one 13-line ground squirrel completed this experiment.

Results

Discrimination performance on this problem is shown for one subject in Fig. 13. Each plotted point in that figure represents the mean for 150 test trials. As can be seen, for each of these test points the animal reached about 80 per cent correct for those discriminations made over substantial spectral regions. For standard wavelengths of 452 and 538 nm, successful discrimination could be obtained from only one spectral direction--toward the long wavelengths for 452 nm, and toward the short wavelengths for the 538 nm standard. The results for both of these latter tests are shown in the upper left-hand panel of Fig. 13. It can be clearly seen from this figure that wavelength discrimination varies as a function of the standard wavelength, and that for a particular standard, the discriminability of adjacent points is not necessarily the same in both directions. Data obtained from the other two subjects were very similar to those shown in Fig. 13. To generate wavelength-discrimination functions, the change in wavelength (AA) from that of the standard (X) required to produce discrimination at the 40 per cent level was calculated for each animal at all of the test locations. The results of these measurements are shown in Fig. 14. For the 471,493 and 506 nm standards, the points in the figure are the means of + Ah and -Ah while the values given for 452 and 538 nm represent discrimination in only one spectral direction. The solid line in the figure represents the location of the mean wavelength discrimination for all three subjects. As Fig. 14 shows, ground squirrels can discriminate between wavelengths over only a relatively restricted portion of the spectrum and this capacity is well developed only over a

530

GERALD H.JA~~BSANDROBERTL.YOLTON

range of some 20 nm or so. The test points were too few to accurately define the spectral location of best wavelength discrimination, but it might be noted here that the animals did at least as well at 493 nm (which is 12 nm from the measured neutral point) as they did at 506 nm which is very close to their spectral neutral point. The wavelen~h-~~rimination function for the ground squirrel is similar in form to the most-frequently reported wavelength-discrimination functions for human observers having protanopic and deuteranopic color vision (PITT, 1935).

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Even though the ground squirrel shows generally poor wavekogth discrimination compared to that of a trichromatic observer, discriminative capacity at the best spectral locations is quite good. For one subject the spectral region around the 493 nm standard was explored in 1 nm steps-this squirrel showed better than chance discrimination for diBerences of 2 nm, which was about as good as a human observer did in the same situation. Discussion

Consideration of the wavelength pairs that were successfully discriminated by the two species of ground squirrels tested here, suggests that they possess color vision which is at leaat grossly similar to that found in some of the other kinds of ground squirrels. Spec&cally, CRESCITELLI and POLUCK (1966) found that the antelope ground squirrel was able to successfully discriminate a light of 460 nm from various other lights all located at 500 nm and beyond; obviously the squirrels tested in this study could perform these same discriminations. On the other hand, the sousliks examined by BONAVENTURE (1959) were successful

Visual Sensitivity and Color Vision in Ground Squirrels

531

in the discrimination of several pairs of wavelengths, including 575 vs. 591 nm and 575 vs. 622 nm. With brightness differences carefully controlled, it seems unlikely that either the 13-line or Mexican ground squirrels would be successful at discriminating these latter test pairs. It is widely recognized that the relevant cue for wavelength discrimination in dichromatic observers includes important contributions from both spectral saturation and hue. Indeed, since the dichromatic individual apparently perceives only two spectral hues, one to either side of the neutral-point (GRAHAMand HSIA, 1958), it is apparent that except for the region close to the neutral-point location, the most likely cue for discrimination is the difference in spectral saturation (HECHT and SHLAER, 1936). Thus the ability of the animals tested here to discriminate 470 from 450 nm, and 538 from 510 nm, is likely based entirely on the use of the differences in spectral saturation produced by these different stimuli.

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FIG.14. Wavelength discrimination for the ground squirrels. The symbols represent individual animals, the solid line the mean for the group.

In view of the potency of saturation differences as a cue for wavelength discrimination, and the fact that the change in dichromatic hue occurs at the neutral-point location, it is to be expected that wavelength discrimination should be maximal at the location of the spectral neutral point. As described above, although the zone surrounding the neutralpoint location was not examined in great detail, it appears that for these squirrels the point of best wavelength discrimination may well be at some wavelength shorter than the measured neutral-point location. Since the stimuli used for measurement of wavelength discrimination will be less affected by intraocular filtering than those used in the neutral-point test, it might be suggested that the neutral point for the ground squirrel, if measured at the retinal level, would be located at a shorter wavelength than that reported in the previous experiment. 4. Chromaticity confusion None of the various indices employed to discriminate among the various types of human dichromacies are entirely unambiguous. However, among these indices, determinations of chromaticity-confusion lines are perhaps the most useful. If various chromaticities

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L. YOLTON

that are indistinguishable to dichromatic observers are joined by straight lines in the CIE calorimetric coordinate system, the directions and points of intersection of groups of such lines are clearly different for the various classes of dichromats (Prrr, 1935). Since, as described above, the locations of the spectral neutral points for the ground squirrels were somewhat puzzling, it was hoped that determinations of chromaticity confusion lines for these animals would shed further light on the nature of their dichromatic color vision. Procedure. The tests to establish points of chromaticity confusion were analogous to the tests used to locate the spectral neutral point, except that the negative stimuli were purple lights rather than white. Confusion points were determined for four different locations selected to cover the range along the purple line of the chromaticity diagram. Characteristics of the filters used to produce these stimuli are given in Table 1. Ground squirrels were initially trained with the monochromator (positive stimulus) set at 440 or 580 nm vs. one of the four negative purples. Brightness equations between the monochromatic and purple lights were established by using the techniques described preyiously. An additional variation of f 0.3 log,, units around each equation value was used. After the subject had reached maximal performance on this initial discrimination, the spectral region between 440 and 580 nm was explored in steps of 10 and 5 nm. The animal was tested over this region many times-30 observations per wavelength were obtained in each test session and thus a substantial portion of the spectrum was examined daily. Subsequently, similar measurements were made for the other three negative stimulus conditions. Data were obtained from three Mexican and two I3-line ground squirrels. TABLE 1. CHARACTERISTICS OF THE FILTERSUSED TO DETERMINE CHROMATUTY

SPECIFICATIONS AREMIRILLUMINANT Filter No.

31 32 34A 34

Chromaticity coordinates X Y 0609 0.541 0.391 0.276

0.262 0.228 O-129 0.069

MATCHES.

A Excitation purity

80.0 77.0 94.0 91.5

Results

The discrimination between extraspectral and spectral stimuli was an obviously di5cult task for the ground squirrel as the maximal performance after substantial training seldom exceeded the level of 60 per cent correct. Nevertheless, all animals were able to achieve about this level of performance for the discriminations of 440 and SO urn against each of the negative stimuli. At spectral points intermediate to these two locations, discrimination Ievels remained about the same except over a zone of some 25 nm where the level of performance gradually fell off and reached chance at some point-the location of this zone was different for the four stimuli tested. (If any further evidence is needed, the fact that discrimination did drop to chance levels for each of the test conditions also indicates these animals are dichromats.) After an animal’s discrimination performance showed no further change, an additional 120 observations per spectral point were collected; from these results a “match” point was determined by taking the midpoint of the spectral range over which discrimination did not exceed 40 per cent correct. These match points are shown in Fig. 15 where, in CIE chromaticity coordinates, lines have been drawn to connect the matched pairs and then extended so as to intersect the spectrum locus or its extension. In this figure, the matches for four animals are shown for each test condition. As can be seen, the spectral range of the match points is relatively restricted across subjects-the range does not exceed 9 nm except for the 34A

VisualSensitivityand Color Visionin Ground Squirrels

533

filter which produced a spread of 17 nm across subjects. It might be noted that, even for the best conditions, the range of match points is more than twice as large as the range of spectral neutral points for these squirrels. There were no systematic differences in match location attributable to the species of the squirrel.

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FIG. 15. Chromaticityconfusion lines obtained from four ground squirrels.Match results are shown for tests against four different filters. For each filter a straight line has been drawn to connect

the spectral match point, the chromaticity coordinates of the test filter, and the spectrum locus or its long wavelength extension.

The mean chromaticity confusion lines generated from the results of this experiment are shown in Fig. 16. All of these lines converge toward a region close to the long-wavelength spectrum locus. They do not, however, converge to a single point. For human dichromats the confusion lines for the deuteranopic individual converge gradually, while those for the protanopic observer converge sharply on roughly the same region as that shown in Fig. 16 (Prrr, 1935). The dichromacy of the ground squirrel is apparently closer in character to that shown by the human protanope than to that of the other human dichromats. Discussion

Plots of chromaticity confusion lines have received much attention from color vision theorists since, in the view that dichromacy occurs as a reduction from trichromacy, the locus of convergence of the confusion lines represents the chromaticity coordinates of the

GERALD

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H. JACOBSAND ROBERT L. YOLTON

missing color process. Figure 16 shows that the chromaticity confusion lines generated by the ground squirrels run in the same direction as do the lines obtained from protanopic humans. These lines do not, however, converge on a single point in the chromaticity diagram. In this regard, it should be pointed out that there is evidence to suggest that the convergence of confusion lines for human dichromats is seldom as clear cut or as universal as it is classically represented to be (FARNSWORTH,1961; SCHEIBNER and BOYNTON,1968). In spite of the lack of complete convergence of the confusion lines drawn for the ground squirrel, it is possible to estimate the region of convergence (the copunctal point). One way to do this is to take the location of intersection for every pair of lines; the mean location for such intersections for the ground squirrel is at, X=0*70, Y=O*26. Alternatively, the

0.6 Y

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points of inters&ion of each line with the spectrum locus or ita long-wavelength extension can be used as an estimate. The mean locution for the four intersectiona de&m&d in this way is at, X10-74, Y=O*25. The copuoctal point obtained for human protanopes in two extensive experiments was at, X=&74, Y-O*25 (JUDD, 1966) and thus the results of chromaticity matches from the ground squirrels are approximately the same at the matches obtained from human protanopes. CONCLUDING

COMMENTS

The experiments reported here provide a reasonably clear picture of several of the basic visual capacities of theground squirrel. Ofperhapsgrcatest interest is the evidence for a color vision in these species that is similar in character to that of the human protanope. Among

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mammals, only a few species have been sufficiently investigated to permit a characterization of their color vision and, of these, probably not more than four species can be clearly identified as possessing color vision different from that of the normal human. Both squirrel monkeys (JACOBS,1963) and Cebus monkeys (DE VALOIS,1965; GUNTER, FEIGENSONand BLAKESLEE, 1965) are anomalous trichromats, while the tree shrew is dichromatic (POLSON, 1968). To this short list the cat should probably also be added, although the nature of its color vision relative to the human classification scheme is still unclear (DAW and PEARLMAN, 1969). To this group, Mexican and I3-line ground squirrels can now be added as dichromats. In the light of the results on the ground squirrel, recent experiments on the tree shrew, Tupaia, are especially interesting. Z’upaia, like the ground squirrel, has an all-cone retina. POLSON’S(1968) extensive series of experiments on Tupaia showed this animal to have dichromatic color vision, the dichromacy being similar to that of the human deuteranope. Thus both of the genera having all-cone retinas which have been investigated have been found to be dichromatic. One can but wonder if other animals having all-cone retinas are also dichromatic and, if so, why it should be that such specialized retinas have been limited to the elaboration of only two classes of photopigment. A final comment concerns the applicability of the classification schemes developed to describe human color vision for the study of animal color vision. In the experiments reported here, ground squirrels were found to have color vision similar to that expected of a human protanope. However, the peak of the luminosity function, the neutral-point location, and the lack of convergence of the isochromatic lines for these animals all differ somewhat from the picture classically drawn for human protanopic vision. These discrepancies are certainly not surprising in view of the differences in intraocular absorption between ground squirrel and man and, indeed, in the fact that their respective retinal photopigments seem to show peak absorption at different spectral locations. It thus seems clear that to describe ground squirrels as protanopic may well be to obscure some of the essential features of their color vision. Similar differences are also evident in the comparisons made between tree shrews and human deuteranopes (POLSON,1968). As our information about comparative color vision expands it may be well to keep in mind that the extension of the human classification schemes provides a convenient shorthand but not necessarily an accurate descriptor. Acknowledgmenrs-This research was supported by Grant EY 00105 from the National Eye Institute. We thank DENNISMCFADDENfor his comments on the manuscript.

REFERENCES ARDEN, G. B. and TANSLEY,K. (1955). The spectral sensitivity of the pure-cone retina of the souslik (Citellus citellus L.). J. Physiol130, 225-232. BONAVENIIJRE,N. (1959). Sur la sensibilitt spectrale el la vision des couleurs chez le spermophile (Cifellus citellus L.). C.r. Sot. Biol., Paris 153, 1594-1597. BORNSCHEIN,H. (1954). Elektrophysiologischer Nachweis einer I-Retina bei einem Saiiger (Cite//us cite//us L.). Naturwissenschaffen, 41,435-436. CRFSCITELLI,F. and POLLACK,J. D. (1965). Color vision in the antelope ground squirrel. Science, N. Y. 150, 13161318. CRESC~TELLI, F. and POLLACK,J. D. (1966). Investigations into colour vision of the ground squirrel. In Aspects of Comparative Ophthalmology, pp. 41-55, Pergamon Press, Oxford. DARTNALL,H. J. A. (1953). The interpretation of spectral sensitivity curves. Br. med. Bull. 9, 24-30. DAW, N. W. and PEARLMAN,A. L. (1969). Cat colour vision: One cone process or several? J. Physiol. 201, 745-764. DE VAU)IS, R. L. (1965). Behavioral and electrophysioIogica1 studies of primate vision. In Contributions to Sensory Physiology, Vol. 1, pp. 137-178, Academic Press, New York. DE VALOIS,R. L. and JACOBS,G. H. (1968). Primate color vision. Science, N. I’. 162, 533-540.

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DOWLING,J. E. (1964). Structure and function in the all-cone retina of the ground squirrel. In The Physioiogical Basis for Form Discriminatian, pp. 17-23, Brown University, Providence. FARNSWORTH, D. (1961). Let’s look at those isochromatic lines again. Vision Res. 1, l-5. GRAHAM,C. H. and Hsu, Y. (1958). Color defect and color theory. Science, N. Y. 127, 675-682. GRETHER,W. F. (1939). Color vision and color blindness in monkeys. Comp. Psychol. Monogr. 15, l-38. GUNTER,R., FEIGENSON, L. and BLAKESLEE, P. (1965). Color vision in the Cebus monkey. J. camp. Physiol. Psychol., 60, 107-113. HECHT,S. and SHLAER,S. (1936). The color vision of dichromats-II. Saturation as a basis for wavelength discrimination and color mixture. 1. gen. Physiof. 20, 83-94. HOWELL,A. H. (1938). Revision of the North American GroundSquirrels, U.S. Dept. of Agriculture, Washington, D.C. JACOBS,G. H. (1963). Spectral sensitivity and color vision of the squirrel monkey. J. camp. Physiof. Psychol. 56,616621.

JACOBS,G. H. and YOLTON,R. L. (1969). Dichromacy in the ground squirrel. Nature, Land. 223,414-415. JVDD,D. B. (1944). Standard response functions for protanopic and deuteranopic vision. J. res. natl. Bur. Stand. 33, 404-437. JUDD,D. B. (1966). Fundamental studies of color vision from 1860 to 1960. Proc. natl. Acad. Sci., U.S.A. 55.1313-1330.

KOWVARY, G. (1934). A study of color vision in the mouse (Mus musculus 1.) and the souslik (Citelhts cite&s L.). J. gem?. Psychal. 44,473-477. LINSDALE, J. M. (1946). 27te Corifortia Ground squirrel, University of California Press, Berkeley. MICHAEL,C. R. (1965). Receptive fields of si@e optic nerve fibers in the ground squirrel. Doctoral thesis, Harvard University. MICHAEL,C. R. (1968). Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. J. Neurophysiol. 31, 249-282.

PAK, W. L. and EBREY,T. G. (1966). Early receptor potentials of rods and cones in rodents. J. gen. Physiol. 49, 1199-1208. Ptrr, G. H. C. (1935). Characteristics of dichromatic vision. Med. Res. Counc., Special Rep. Series. 200, pp. l-58. POLSON, M. C. (1968). Spectral sensitivity and color vision in Tupaiaglis. Doctoral thesis, Indiana University. SCXEIBNER, H. and B~YNT~N,R. M. (1968). Residual red-green discrimination in dichromats. J. opt. Sot. Am. 58, 1151-1158.

SPERLING,H. G., SIDLEY,N. A., DOCKENS,W. S. and JOLLIFFE,C. L. (1968). Increment-threshold spectral sensitivity of the rhesus monkey as a function of the spectral composition of the background field. J. opt. Sot. Am. 58,263-268.

TANSLEY, K. (1961). Comparative anatomy of the mammalian retina with respect to the electroretinographic response to light. In The Structure of the Eye, pp. 193-206, Academic Press, New York. TANSLEY, K., COPENHAVER, R. M. and GUNKEL,R. D. (196la). Some observations on the off-effect of the mammalian cone electroretinogram. J. opt. Sot. Am. 51, 207-213. TANSLEY, K., C~PENHAVER, R. M. and GUNKEL,R. D. (196lb). Spectral sensitivity curves of diurnal squirrels. Vision Res. 1, 154-165.

VAIDYA,P. G. (1964). The retina and optic nerve of the ground squirrel Citellus tridecemlineatus tridecemlineatus. J. wmp. Neural. U&347-354.

V~LTER,V. (1954). Histologie et activite electrique de la retine d’un Mammifere strictement diume, le spermophile (Citellus citellus). C. r. Sot. Biol., Paris 148, 1768-1771. WALLS,G. L. (1931). The occurrence of colored lenses in the eyes of snakes and squirrels, and their probable signiticance. Copeia 125-127. Wuts, G. L. (1940). The pigment of the vertebrate lens. Science, N. Y. 91,172. WALLS,G. L. (1941). The Vertebrate Eye, The Cranbrook Institute of Science, Bloomfiald Hills, Michigan. WALLS,G. L. and HEATH,G. G. (1956). Neutral points in 138 protanopes and deuteranopes. J. opt. Sot. Am. 46640-649.

Abstract-Several measures of visual capacity were obtained from ground squirrels (Citellus mexicanus and Citelfus tridecemfineatus) in discrimination tests. These measures included: (a) spectral sensitivity functions for conditions of achromdc and chromatic adaptation, (b) dark-adaptation functions, (c) tests for a neutral point, (d) wawh dbcrimirution, and (e) chromaticity confusion lines. The all-cone character of vision In these animals is expm in the lack of any shift in relative spectral sensitivity as a&mm&c adaptation state is altered and also in the rapid and relatively small mcrcase in sensitivity during dark adaptation. More than one prcass was found to underlie ths epe&al sa&tivity function. These squirrels have color vision of the dichromatic variety with a well-de&ed neutral point. Their wav&ngthdiscriminating abilities are also characteristically dichromatic. Measumments of chromaticity-

Visual Sensitivity and Color Vision in Ground Squirrels

confusion loci suggest that the dichromacy of these squirrels is closest to that shown by protanopic humans. No differences were found between these two species of ground squirrel on any of the measures of visual capacity.

Resum&-Gn

obtient par des tests de discriminatibn diverses mesures de la capacite visuelle d’&cureuils terrestres (Citehs mexicanus et Citellus tridecemlineatus). Ch mesures comprennent : (a) les fonctions de sensibilite spectrale en adaptation achromatique et chromatique,

(b) les fonctions en adaptation a l’obscurite, (c) la recherche du point neutre, (d) la discrimination en longueur d’onde et (e) les lignes de confusion chromatique. Le fait que la &tine de ces animaux ne contienne que des cbnes explique I’absence de decalage dans la sensibilite spectrale relative quand on change l’dtat d’adaptation achromatique ainsi que l’accroissement rapide et relativement faible de la sensibilite durant l’adaptation a l’obscurite. La fonction de sensibilite spectrale met en jeu plus d’un m&a&me. Ces ecureuils ont une vision color&e du type dichromate avec un point neutre. bien dC6ni. Leurs possibilitea de discrimination chromatique caract&isent aussi les dichromates. Les lieux de confusion suggerent que le dichromatisme:de ces ecureuils est proche des protanope-s humains. On n’a constate aucune difference entre les deux esp&ces d’Bcureui1 terrestre dans les mesures de capacitt visuelle.

Znsammenfass~g-Das Unterscheidungsvermbgen des Zirsels (Citellus mexicanus und Citellus tridecemlineatus) wurde beniitzt, urn die folgenden Masse ihrer SehstArke zu gewinnen: (a) Spektralemptindlichkeitsfunktionen unter farblosen und farbigen Redingungen, (b) die Dunkeladaptierung, (c) Versuche 6be.r den Graupunkt, (d) das Wellenlringenunterscheidungsvermogen und (e) die Linien der Chromatizitatsverwechslung. Die reine Zapfenart des Sehens dieser Tiere wird durch die Abwe-senheit jeglicher Verschiebung der relativen Spektralempfindlichkeit wahrend der farblosen Umstimmung und such durch die schnelle und verhlltnism%ssig kleine Emptindlichkeitserh6hung wlhrend der Dunkeladaptierung ausgedrtickt. Der

Spektralemptindlichkeitsfunktion unterliegen mehrere Mechanismen. Diese Zirsel besitzen ein dichromatisches Farbensehen mit einem gut gekennzeichneten Graupunkt. Ihr Wellenllngenunterscheidungsverm6gen ist such typisch dichromatisch. Messungen der Chromatizitltsverwechslungslinien legen es nahe, dass die Dichromatic dieser Zirsel der menschlichen Protanopie ahneln. Es wurden keine Tierartsunterschiede in irgendeinem Masse der Sehkraft gefunden. Pe3ro~+Y cnoMnrbt0

cycnri~os 6binH npoE3BeAeHbr HeKoTopble a3MepeHHs 3prr~em&toHcnoco6HocTH Tecro~ na pa3mireHTre. &.mi EccnenoBaaaa Citellw mexicanus H Citellus tridecemlineatus. 3ra Hwepewfn BKJIKIY~HH: (a) (P~HKIJEEcnexrpam,nonryser.rsrn.renr, HocTE LUUlyeJIOBti aXpOMaTHYeCKOtiH XpOhfaTH’IeCKOHaAartTanHH, (6) r&KHHHHTeMHOBOH aAarrranmi (B) HcuteAoBaHmr He&rpaAbxoro nyHKTa B cnerrrpe, (r) pa3mrreHrie ~nmi BOAH cnetcrpa, H (A) nymc~bt cnexrpa, usera K0~0pbM nyTatoTca. fIomiocr~40 KOA~O~KOB~I~~ xapaKTep sperms ~THX XO~BOTHM~ BblpaXcaeTcKB OTC~TCTBHHKaKOrO ~~60 CABHTaB OTHOcHTertbHot4cneKTpaHot HyBcrBHTenbHom~t,cum ri3MeHKeTcs cocrosmrie axpohrarwecxol ananraumi, a rate xce B ~~ICT~M H onwc~w.JIbHo He6onbmoM ynenmeHHrf Hy~crnHTeJtbAOCTHnpE TeMHOBOHaAatrTaHHE. @yHKHHK) ClTeKTpaAbHOH‘ryBCTnHTeJrbHOCTH 06ycnoBJtHBaeT6onee 4eM OAHH npOHecc. %H CyCAHKH06AaAamT AHXpOMaTHYeCKHM HBeTOBbtM 3peHrieM, c xopomo 0npeAeneHAbtM HettTpannHMMnyri~~o~. Mx c~1oco6~oc~~ piurrwernin Amm Bomi ~BAR~~TCKTaK xe xapaxrepao mpohrarmtecrcnMH. Onpenenesme nHKKTOBB CUeKTpe, rAe JJBeTaCMelItHBaK)TCayKa3blBaEOTHa TO, YTO y 3THx CyCllHKOBAHXpOMa3Hs BJWKO HanoMmraeT npo~a~on~ro nenonexa. IIprr nsr+reperrnn mo6ofi ~3 &~~mrti 3pemra y

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