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Near-field visual acuity of pigeons: Effects of scotopic adaptation and wavelength
Printed
in Great
Britain.
VISUAL ACUITY OF PIGEONS: EFFECTS OF SCOTOPTC ADAPTATION AND WAVELENGTH WILLIAM Hews
and
ROSALIND
W.
LEIBOWITZ
Department of Psychology,
University of Maryland, College Park, MD 20742, USA.
(Received
27 June 1976; in revised form
1 August 1976)
Abstract-Pigeons were trained to perform in a visual acuity task. In the first experiment, two pigeons were tested at each of four values of target luminance under conditions of scotopic adaptation. Acuity de&ted as a function of target tuminance. At comparabie values of target luminance, scotopic acuity was approx SO:/, of photopic acuity. In the second expe~ment, three photopi~lly-a~pted pigeons were tested with the stimuIus illuminant confined to each of four wavelength bands. Acuity was highest in the spectral band with a dominant wavelength of 575 nm and lowest in the band with a dominant wavelength of 458 nm. Key Words-pigeon;
luminance; scotopic adaptation; wavelength; visual acuity.
Recent studies have investigated the visual acuity of various birds under differing conditions of adaptation and target luminance (P. M. Blot@, 1971, 1973; Fite, 1973; Fite, Stone and Conley, 1975; Martin and Gor-
don, 1974; Hodos, Leibowitz and Bonbright, 1976; Fox, Le~kuhle and W~tendorf~ 1976). In the most recent of these Hodos et al. (19761 jnvesti~ated the visual acuity of pigeons as a function of target luminance. The illumination in the test chamber maintained the birds under conditions of photopic adaptation (ID. S. Blough, 1956) as the target luminance was varied. The results indicated that the pigeons’ acuity was highest at approx 2.3 log cd/m’. Further increases in target luminance resulted in a fall-off of acuity. At the low-luminance end of the function, the birds ceased r~~onding to the stimuIi when the target luminance was less than -0.07 log cd/m’, which suggested that the photopically adapted pigeon was unabIe to detect lower-lumin~~ targets. The present e~~riment was carried out in order to investigate the visual acuity of pigeons under conditions of scotopic adaptation. METHOD
Subjects The subjects were two white Carneaux pigeons, Colt&a Eivia, obtained from the Palmetto Pigeon Plant, Sumter, S.C. The birds were 6 and 8 yr old at the start of the experiment and had been used as subjects in previous studies of visual acuity (Hodos et al., 1976). During the course of the experiment, the pigeons were maintained at 7580% of their free-feeding weights,
a series of square-wave gratings (Ronchi rulings) that ranged in spatial frequency from t to 12 Iines/mm and in contrast from 98.9 to 96.8%. An additional grating with spatial frequency of 0.4 lines/mm and contrast of 89.6X was made by photographically enlarging one of the higherfrequency gratings on high-contrast film. Each grating was paired with a Bausch & Lomb glass, neutral-density fEter of nominal optical density of 0.3, referred to hereafter as the “blank stimulus”. Microscope cover glasses, ranging in optical density from 0.04 to 0.07 were added either to the gratings or to the neutral-density filters to match the average Iuminance within each stimulus pair to less than 0.02 log unit. The luminance differences between stimulus pairs were less than 0.04 log unit. Two sets of gratings and neutral-density filters were mounted in a filter wheef 7.0 mm behind the front surface of the glass key. A soIenoid-o~rat~ shutter was located between the filter wheel and the rear surface of the key. A ground-glass diffusing screen was located between the filter wheel and the light source, which was a Sylvania CBA projection lamp continuously maintained at 3.5 A. Kodak Wratten No. % neutral-d~sity filters located in the beam path attenuated the ~~in~~ of the target to 1.0 cd/m’. Ad~t~on~ filters were added during individuat sessions to further attenuate the target luminance in increments of 0.5 log unit. The luminances of the keys and the interior walls of the grain hopper were adjusted to be approximately equal to that of the stimulus behind the glass center key by means of neutral density filters and trimming potentiometers. Except for the key and feeder tights, the chamber was dark. Procedure
The procedure was the same as that used by Wodos et al. (1976) to measure the photopic acuity-luminance function in pigeons. Details of the preliminary training of the subjects are given in that article. A trial began with the opening of the shutter. Either the grating or the blank was visible through the plass center key. The subject was Appararfis required to peck the cent$r key 10 times. The tenth peck The apparatus has been described in detail elsewhere resulted in the closing of the shutter and the illumination (Hodos et rd.. 1976). In brief. the ex~~imenta~ cb~~r of the right and left side keys. If the center key had diswas a three-key, pigeon test chamber 6at had been modiplayed the grating, a single peck on the right side key lied to permit light from an externally-located source to resulted in 3-5 see access to the grain dispenser, which fall on the center key. The center key had been fabricated contained mixed grains. If the blank stimulus had been from a microscope slide and was made opaque, except for present on the center key, a single peck on the left side a 1.5 cm circular region in the center. The stimuh were key likewise resubed in access to the g&n dispenser. Thus 463
464
WILLIAII 1+xx~s and ROSALINL>W. LEIBO~ITZ
the birds were required to perform the following conditional discrimination: grating on the center key, peck right side key; blank on the center key, peck left side key, Every correct response was followed by the illumination of the feeder light. but only a random SOT,,of these responses were accompanied by the delivery of grain. Each session began with a block of 14 “warm-up”’ trials of the 0.4 lines/mm gratings vs the blank stimulus, which were not used in the analysis. This was followed by an “assessment” block in which the same stimulus pair was repeated. If the bird made more than two errors during the assessment block, the stimuli remained the same for the remainder of the session, which was recorded as a training session. If the bird performed at 90”,, or better in the assessment block, the psychophysical testing was continued and the data collected during this period were used as the first determination of performance at 0.4 iines~mm. The sequence of blocks of stimulus-pars (grating t’s blank) following the assessment block was carried out in ascending order of spatial frequency. Within each pair. the order of stimulus presentation was determined by a quasi-random sequence (Fellows. 1967). After completion of the series of gratings and blanks, the test sequence including the “warm-up” block was then repeated. The total number of trials for training or testing sessions, including both warm-up blocks, was 336. In both the training and testing sessions, pecks on an incorrect key resulted in a 4.5 set period in which the keys and the chamber were dark and the shutter closed. Pecks on dark keys were ineffective. Following an error, a correction procedure was used in which the previous stimulus was repeated until the bird made the correct response. Error-correction responses were followed by the feeder light. but were never accompanied by the delivery of grain. During each session, the luminance of the center key was 1.0 cd/m2 or was attenuated by one, two or three of the OS neutral-density filters. The data from the first session at each level of target luminance were discarded. Testing was continued at different luminance levels (in quasi-random order) until data had been accumulated from three sessions at each luminance level. Prior to each session the birds were brought into the experimental room and placed in a ventilated cage draped with several layers of black felt cloth for I hr of dark adaptation. D. S. Blough (1956) has reported that the absolute threshold for target luminance reaches a minimum after approx 45 min of dark adaptation. In order to prevent the pigeons from falling asleep during dark adaptation we were obliged to enter the experimental room at 5-10 min intervals during the adaptation period and gently tap on the cage or move it slightly in order to maintain the birds in a state of wakefulness. RESI! LTS
The percentage of correct responses obtained with each stimulus pair was plotted as a function of the spatial frequency of the grating to form a psychometric function. The point of subjective equality was determined by the point at which the psychometric function crossed the 75% correct line, which is halfway between chance performance and perfect detection of the grating. The grating frequency at the point of subjective equality was taken to represent the minimum-separable spatial frequency. The visual-angle subtense of each grating bar at the point of subjective equality was estimated for each subject at each luminance level. In est~ating the angular subtense we assumed that the pigeons viewed the stimuli from the near-point of accommodation. I-Iodos et ul. (1976)
v -1.k
-1.b
-015
0.b
LUMINANCE (log
d.5 cd /m2 )
110
Fig. 1. Visual acuity of two pigeons as a function of target luminance under conditions of scotopic adaptation. Aiso shown is a portion of each pigeon’s photopic acuity-luminance function (Hodos et ai.. 1976).
estimated this distance to be 62 mm based on an analysis of 1000 frame/set motion picture films of pigeons viewing the stimuli in this apparatus and the schematic pigeon eye of ~arsh~1, Mellerio and Palmer (1973). Figure 1 indicates visual acuity (l/visual angle in min) as a function of target luminance. Also shown in the figure are the data of these two pigeons at comparable levels of target luminance under conditions of photopic adaptation (Hodos et ul., 1976). Pigeon C-412 showed a progressive decline in acuity at each successively lower target luminance. Acuity declined to 0.025 corresponding to a visual angle of 40’. Pigeon D-27 showed a lesser rate of decline than did C-412, but at the lowest luminance value, the two birds had nearly the same acuity. D-27’s acuity was 0.028, corresponding to a visual angle of 32’. Comparison of the scotopic and photopic acuity of the pigeons at roughly equal target luminances indicates that scotopic acuity is considerably poorer than photopic acuity. Photopic acuity at -0.07 log cd/m’ was 0.17-0.18, corresponding to visual angles of 5.8-5.6’, respectively. Scotopic acuity at 0.0 log cd/m’ was O.OY&U.Oll, corresponding to visual angles of 10.2-9.2’, respectively. DISCUSSION The psychometric functions indicated that only the 0.4 lines/mm grating could be reliably resolved by either subject at the lowest luminance used. The bar width of these gratings was 2.5 mm, with an angular subtense of 2.3”. At this frequency, only three bar/ space pairs were visible through the 1.5 cm aperture behind the glass center key. Indeed, a smaller number of bars may no longer constitute an adequate representation of a grating (Kelly, 1975; van den Brink and B&en, 1975). The results indicated that at roughly equivalent levels of target luminance (approx 1.Ocd/m2), the scotopically-adapted pigeon retina has approximately
465
Near-field visual acuity of pigeons
half the near-field visual acuity as the photopicallyadapted pigeon. However, since pigeons use different portions of the retina for near and far vision (Millodot and P. M. Blough, 1971; Nye, 1973) with different densities of receptors and ganglion cells (Binggeli and Paule, 1969; Galifret, 1966, 1968) the results might have been different had scotopic far-field acuity been measured in an apparatus similar to that used by P. M. Blough (1971, 1973). The luminance of the target at the rod-cone “break” of the pigeon dark-adaptation function (D. S. Blot@, 1956) was several log units below the “break” suggested by the present data. However, Blough’s experiment investigated the pigeon’s ability to detect a uniformly luminous field and not to resolve a spatial distribution of luminances within that field. The demands of the latter task are considerably greater. Figure 2 summarizes the currently available data on acuity-luminance functions for birds. Shown in the figure are data from pigeons based on the present report and Hodos et al. (1976), the great-horned owl, Bubo virginianus (Fite, 1973), the tawny owl, Strix aluco (Martin and Gordon, 1974), and the falcon, F&o sparverius (Fox et al., 1976). The figure indicates that the photopic acuity of pigeons exceeds that of the two owl species at comparable target luminances. A recent report by Fite et al. (1975) indicated that the upper limit of the acuity-luminance function of the northern blue-jay, Cyanocitta cristata, is similar to that of the pigeon; however, the blue-jays have somewhat higher acuity at the lower luminance levels. Both the tawny owl and pigeon functions show an abrupt fall-off of acuity at high luminances. Fite et al. (1975) reported a similar effect in blue jays. The decline in acuity at high target luminances may represent the effects of glare. -
““1 .2
0 So.
The inset figure indicates that at comparable targetluminance values, falcon acuity exceeds that of pigeons by a factor of about 10. Pigeons and greathorned owls have approximately equal acuity for grating targets with luminance of approx 1 cd/m’. However, the great-horned owl’s acuity is superior to the pigeon’s at lower target luminances under either condition of adaptation. An important consideration in comparing these acuity-luminance functions is that differences in retinal illumination have not been taken into account. If the abscissa represented retinal illumination rather than target luminance some displacement of the curves might have resulted. EXPERIMENT
2
The color vision of birds, particularly pigeons, has been extensively investigated in recent years. In addition to studies of both scotopic and photopic spectral sensitivity (D. S. Blough, 1957; Ikeda, 1965; P. M. Blough, Riggs and Schafer, 1972) investigations have been carried out of pigeons’ ability to discriminate small differences in wavelength and match wavelengths throughout the photopic spectrum (P. M. Blough, 1972; Wright, 1972; Wright and Cumming, 1971). Another series of studies explored possible underlying mechanism of avian color vision in terms of cone pigments and the colored oil droplets contained in the cones (Graf and van Norren, 1974; van Norren, 1975; Mayr, 1972; King-Smith, 1969; Pedler and Boyle, 1969, Sillman, 1969) and the spectral sensitivity of single neurons in the pigeon thalamus (Granda and Yazulla, 1971; Yazulla and Granda, 1973). However, no studies have investigated the visual acuity of birds in different regions of the photopic spectrum. The experiment reported here investigated the near-field visual acuity of pigeons with the illuminant confined to one of four relatively narrow bands of-the photopic spectrum. The results obtained were similar to data obtained from human observers.
045
METHOD
04D-
Subjects The subjects were the same as in experiment
0.35 3 p.30-
< ci f.
Y
1 42 0 F
0.2s 2 i 50.20-
5:
0.1%
0.1 o-
IO
0.05-
20 zcl 00
Fig. 2. Visual acuity of several species of birds as a function of target luminance.
1 with the addition of a third pigeon of similar age and experience in visual acuity experiments. Apparatus
The apparatus was the same as that reported in experiment 1, with the following modifications: (1) the grating stimuli ranged in spatial frequency from 2 to 24 lines/mm and in contrast from 98.9 to 93.7%. (2) During each experimental session, one of four narrow-pass, Kodak Wratten color filters was present in the beam path. Kodak Wratten No. 96, neutral-density filters were used to equate the chromatic filters for brightness based on heterochromatic brightness matches by pigeons reported by Hodos (1969). The Kodak Wratten filters that were used are listed below. The dominant wavelength of each filter and the optical density of the neutral density filter that was added to it are given in parentheses. No. 26 (619 nm + 1.0 n.d.); No. 73 (575 nm + 0.6 nd.); No. 93 (545 nm + 0.6 n.d.); No. 94 (458 nm + 0 n.d.). (3) The luminance of the stimulus field on the center key, with no filters in the beam path was 3.65 log cd/m2. (4) The overall chamber illumination was 171 lx and was
466
WILLIAM
HODOSand ROSAUNDW. LEIBOWITZ
produced by two ceiling-mounted, daylight, fluorescent lamps (General Electric F6T.5~CW-HH) diffused by a sheet of translucent plexiglass. (5) The chamber remained illuminated throughout the session. Procedure
The procedure was the same as in experiment 1. Prior to each session, one of the Wratten color filters was placed in the beam path: A different filter was used each day. The data collected during the first session with each filter were discarded. Testing was continued until data were collected from three sessions with each color filter. In order to obtain some data on human performance in this apparatus, which could be compared to the pigeons’ performance, two human subjects were tested. Each subject viewed the gratings through a 5 mm hole in the rear wall of the pigeon chamber. Their heads were maintained in position by a chin and forehead support frame. Push buttons were substituted for the keys and the feeder light provided feedback for correct responses. Each subject was tested for one session with each filter. The filters had been matched by the subjects for brightness by the addition of neutral density filters.
RESULTS Figure 3 presents the visual acuity (l/visual angle in min) of each pigeon as a function of the dominant
wavelength of the illuminant. In each case, peak acuity occurred when the 575 nm illuminant was used. These values ranged from 0.28 to 0.32, corresponding to visual angIes of 3.6-3.2’, respectively. Modest declines from these peak values were observed when the 619 and 545 nm illuminants were used. However, with the 458 nm illuminant, a sharp loss of acuity was observed. The acuity estimates of the subjects tested with this illuminant ranged from 0.076 to 0.090 corresponding to visual angles of 13.2-11.1: respectively. DISCUSSION
The results of this experiment pigeons had a peak acuity when nant was used. All three subjects of acuity at longer and shorter
indicated that the the 575 nm illumishowed a reduction wavelengths. These
3
0 30.
i
a. G 25Ir : 4 GZO4" 2 G 15; 0.10.
ii,
54% DOMINANT
.
v
c-412
-
c-580
c---L
D-27
5kD WAVELEtU3TH
six, (nm)
Fig. 3. Visual acuity of three pigeons as a function of the dominant wavelength of the illuminant.
460
500 WAVELENGTH
600
.
760
(nm)
Fig. 4. Acuity-wavelength functions of pigeons compared with similar functions obtained from two human subjects tested in the same apparatus and from the literature (Cavonius, 1967; Adrian, 1970).
data are roughly comparable in form to data obtained from human subjects in other laboratories, as well as from the human subjects in our laboratory tested with the pigeon apparatus. Figure 4 presents a comparison of the human and pigeon data. The data of Adrian (1970) are based on the detection of Landolt rings. Also shown in this section are the data from our two human subjects tested in the pigeon apparatus. The data from our human subjects are roughly similar to those reported by Cavonius (1967) for grating acuity. Those of the pigeons seem to be somewhat more comparable to those of Adrian (1970) for humans viewing Landolt rings. The similarity of human and pigeon spatial resolution at different wavelengths is surprising in view of the apparent differences in cone structure and photopigments (Graf and van Norren, 1974; van Norren. 1975, Mayr, 1972; King-Smith, 1969; Pedler and Boyle, 1969; Sillman, 1969). On the other hand, except for increased sensitivity to short wavelengths, pigeon and human photopic spectral sensitivity curves are quite similar (D. S. Blough, 1957: Ikeda, 1965; P. M. Blough et al., 1972). One of the principal differences between the avian and human retinas is the presence of colored oil droplets between the inner and outer segments of the majority of cones in the avian retinas (King-Smith, 1969; Pedler and Boyle, 1969; Mayr, 1972). The droplets are red, orange, yellow and colorless. The various droplets are not uniformly distributed throughout the retina. The region corresponding to the binocular field contains an exceptionafly high concentration of red and yellow droplets. This region has a reddish appearance in fresh preparation and is known as the red field. Since the binocular field is the field used for near vision (P. M. Blough, 1971, 1973; Catania, 1964; Millodot and Blough, 1971; Nye, 1973; Hodos et al., 1976) the high concentration of red and yellow droplets may have had an influence on the results. This could be tested by determining the effects of
Near-field visual acuity of pigeons wavelength on far-field acuity using a technique lar to that of P. M. Blough (1971, 1973).
simi-
Acknowledgements-The authors thank K. V. Fite, A. M. Granda and C. R. Cavonius for their valuable comments on the manuscript, S. Weiss and K. Macko who assisted in the collection of the human data, Janice Wilberger who prepared the manuscript for publication and the National Eye Institute, which supported this research through grant number EY-00735. REFERENCES
Adrian W. (1970) Neuere Untersuchungen der spektralen sehscharfe und ihre Bedeutung ftir das Farbensehen. AIC Color 69, Vol. 2. Musterschmidt, Gottingen. Binggeli R. L. and Paule W. J. (1969) The pigeon retina: quantitative aspects of the optic nerve and ganglion cell layer. J. camp. Neural. 137, 1-18. Blough D. S. (1956) Dark adaptation in the pigeon. J. camp. physiol. Psychol. 49. 425430. Blough D. S. (1957) Spectral sensitivity in the pigeon. J. opt. Sot. Am. 47, 823-833. Blough P. M. (1971) The visual acuity of the pigeon for distant targets. J. exp. Analysis Behav. 15, 5768. Blough P. M. (1972) Wavelength generalization and discrimination in the pigeon. Percept. Psychophys. 12, 342-348. Blough P. M. (1973) Visual acuity in the pigeon. II: Effects of target distance and retinal lesions. J. exp. Analysis Behao. 20, 333-343. Blough P. M., Riggs L. A. and Schafer K. L. (1972) Photopic spectral sensitivity determined electroretinographitally for the pigeon eye. Vision Res. 12. 477485. Catania A. C. (1964) On the visual acuity of the pigeon. J. cup. Analysis Behan. 7, 361-366. Cavonius C. R. (1967) The effect of wavelength on visual acuity. Final Contract report, U.S. Army DA-40-193-MD-2839. Fellows B. J. (1967) Chance stimulus sequences for discrimination tasks. Psychol. Bull. 67, 87-92. Fite K. V. (1973) Anatomical and behavioral correlates of visual acuity in the great horned owl. Vision Res. 13, 219-230. Fite K. V., Stone R. J. and Conley M. (1975) Visual acuity in the nothern blue jay: behavioral and anatomical correlates. Neurosci. Abstr. 1, 82. Fox R., Lehmkuhle S. W. and Westendorf D. H. (1976) Falcon visual acuity. Science 192, 263-265. Galifret Y. (1966) Le systbme visuel du pigeon: anatomie et physiologie correlations psychophysiologiques. Doctoral Thesis, Faculty of Sciences, University of Paris.
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Galifret Y. (1968) Les diverses aires fonctionnelles de la retine du pigeon. Z. Zellforsch 86, 535-545. Graf V. and van Norren D. (1974) A blue sensitive mechanism in the pigeon retina: 1 max 400 nm. Vision Res. 14, 1203-1209. Granda A. M. and Yazulla S. (1971) The spectral sensitivity of single units in the rotundus of pigeon (Columba liuia). J. gen. Physiol. 57, 353-384. Hodos W. (1969) Color discrimination deficits after lesions of the nucleus rotundus in pigeons. Brain Behav. Euol. 2. 1855200. Hodos W., Leibowitz R. W. and Bonbright J. C. (1976) Near-field visual acuity of pigeons: effects of head position and stimulus luminance. J. exp. Analysis Behao. 25, 129-141. Ikeda H. (1965) The spectral sensitivity of the pigeon. Vision Res. 5, 19-36. King-Smith P. E. (1969) Absorption spectra and function of the coloured oil drops in the pigeon retina. Vision Res. 9, 1391-1399. Kelly D. H. (1975) How many bars make a grating? Vision Res. 15, 625626. Marshall J., Mellerio J. and Palmer D. A. (1973) A schematic eye for the pigeon. Vision Res. 1, 24492453. Martin G. R. and Gordon I. E. (1974) Visual acuity in the tawny owl (Strix aluco). Vision Res. 14, 1393-1397. Mayr I. (1972) Verteilung, Lokalisation und Absorbtion der Zapfenolkugeln bei Vijgeln (Ploceidae). Vision Res. 12, 1477-1484. Millodot M. and Blough P. M. (1971) The refractive state of the pigeon eye. Vision Res. 11, 1019-1022. Nye P. W. (1973) On the functional differences between frontal and lateral visual fields of the pigeons. Vision Res. 13, 559-574.
Pedler C. and Boyle M. (1969) Multiple oil droplets in the photoreceptors of the pigeon. Vision Res. 9, 525-528. Sillman A. J. (1969) The visual pigments of several species of birds. Vision Res. 9, tQ63-1077. van den Brink G. and Bilsen F. A. (1975) The number of bars that makes a grating for the visual system: a reply to Dr. Kellv. Vision Res. 15. 627-628. van Nbrren D. (1975) Two short wavelength sensitive cone systems in pigeon, chicken and daw. Vision Res. 15, 11641166. Wright A. A. (1972) Psychometric and psychophysical hue discrimination functions for the pigeon. Vision Res. 12, 1447-1464. Wright A. A. and Cumming W. W. (1971) Color-naming functions for the pigeon. 1. exp. Analysis Behau. 15, 7-17. Yazulla S. and Granda A. M. (1973) Opponent-color units in the thalamus of the pigeon (Columba liuia). Vision Res. 13, 1555-1564.
in Great
Britain.
VISUAL ACUITY OF PIGEONS: EFFECTS OF SCOTOPTC ADAPTATION AND WAVELENGTH WILLIAM Hews
and
ROSALIND
W.
LEIBOWITZ
Department of Psychology,
University of Maryland, College Park, MD 20742, USA.
(Received
27 June 1976; in revised form
1 August 1976)
Abstract-Pigeons were trained to perform in a visual acuity task. In the first experiment, two pigeons were tested at each of four values of target luminance under conditions of scotopic adaptation. Acuity de&ted as a function of target tuminance. At comparabie values of target luminance, scotopic acuity was approx SO:/, of photopic acuity. In the second expe~ment, three photopi~lly-a~pted pigeons were tested with the stimuIus illuminant confined to each of four wavelength bands. Acuity was highest in the spectral band with a dominant wavelength of 575 nm and lowest in the band with a dominant wavelength of 458 nm. Key Words-pigeon;
luminance; scotopic adaptation; wavelength; visual acuity.
Recent studies have investigated the visual acuity of various birds under differing conditions of adaptation and target luminance (P. M. Blot@, 1971, 1973; Fite, 1973; Fite, Stone and Conley, 1975; Martin and Gor-
don, 1974; Hodos, Leibowitz and Bonbright, 1976; Fox, Le~kuhle and W~tendorf~ 1976). In the most recent of these Hodos et al. (19761 jnvesti~ated the visual acuity of pigeons as a function of target luminance. The illumination in the test chamber maintained the birds under conditions of photopic adaptation (ID. S. Blough, 1956) as the target luminance was varied. The results indicated that the pigeons’ acuity was highest at approx 2.3 log cd/m’. Further increases in target luminance resulted in a fall-off of acuity. At the low-luminance end of the function, the birds ceased r~~onding to the stimuIi when the target luminance was less than -0.07 log cd/m’, which suggested that the photopically adapted pigeon was unabIe to detect lower-lumin~~ targets. The present e~~riment was carried out in order to investigate the visual acuity of pigeons under conditions of scotopic adaptation. METHOD
Subjects The subjects were two white Carneaux pigeons, Colt&a Eivia, obtained from the Palmetto Pigeon Plant, Sumter, S.C. The birds were 6 and 8 yr old at the start of the experiment and had been used as subjects in previous studies of visual acuity (Hodos et al., 1976). During the course of the experiment, the pigeons were maintained at 7580% of their free-feeding weights,
a series of square-wave gratings (Ronchi rulings) that ranged in spatial frequency from t to 12 Iines/mm and in contrast from 98.9 to 96.8%. An additional grating with spatial frequency of 0.4 lines/mm and contrast of 89.6X was made by photographically enlarging one of the higherfrequency gratings on high-contrast film. Each grating was paired with a Bausch & Lomb glass, neutral-density fEter of nominal optical density of 0.3, referred to hereafter as the “blank stimulus”. Microscope cover glasses, ranging in optical density from 0.04 to 0.07 were added either to the gratings or to the neutral-density filters to match the average Iuminance within each stimulus pair to less than 0.02 log unit. The luminance differences between stimulus pairs were less than 0.04 log unit. Two sets of gratings and neutral-density filters were mounted in a filter wheef 7.0 mm behind the front surface of the glass key. A soIenoid-o~rat~ shutter was located between the filter wheel and the rear surface of the key. A ground-glass diffusing screen was located between the filter wheel and the light source, which was a Sylvania CBA projection lamp continuously maintained at 3.5 A. Kodak Wratten No. % neutral-d~sity filters located in the beam path attenuated the ~~in~~ of the target to 1.0 cd/m’. Ad~t~on~ filters were added during individuat sessions to further attenuate the target luminance in increments of 0.5 log unit. The luminances of the keys and the interior walls of the grain hopper were adjusted to be approximately equal to that of the stimulus behind the glass center key by means of neutral density filters and trimming potentiometers. Except for the key and feeder tights, the chamber was dark. Procedure
The procedure was the same as that used by Wodos et al. (1976) to measure the photopic acuity-luminance function in pigeons. Details of the preliminary training of the subjects are given in that article. A trial began with the opening of the shutter. Either the grating or the blank was visible through the plass center key. The subject was Appararfis required to peck the cent$r key 10 times. The tenth peck The apparatus has been described in detail elsewhere resulted in the closing of the shutter and the illumination (Hodos et rd.. 1976). In brief. the ex~~imenta~ cb~~r of the right and left side keys. If the center key had diswas a three-key, pigeon test chamber 6at had been modiplayed the grating, a single peck on the right side key lied to permit light from an externally-located source to resulted in 3-5 see access to the grain dispenser, which fall on the center key. The center key had been fabricated contained mixed grains. If the blank stimulus had been from a microscope slide and was made opaque, except for present on the center key, a single peck on the left side a 1.5 cm circular region in the center. The stimuh were key likewise resubed in access to the g&n dispenser. Thus 463
464
WILLIAII 1+xx~s and ROSALINL>W. LEIBO~ITZ
the birds were required to perform the following conditional discrimination: grating on the center key, peck right side key; blank on the center key, peck left side key, Every correct response was followed by the illumination of the feeder light. but only a random SOT,,of these responses were accompanied by the delivery of grain. Each session began with a block of 14 “warm-up”’ trials of the 0.4 lines/mm gratings vs the blank stimulus, which were not used in the analysis. This was followed by an “assessment” block in which the same stimulus pair was repeated. If the bird made more than two errors during the assessment block, the stimuli remained the same for the remainder of the session, which was recorded as a training session. If the bird performed at 90”,, or better in the assessment block, the psychophysical testing was continued and the data collected during this period were used as the first determination of performance at 0.4 iines~mm. The sequence of blocks of stimulus-pars (grating t’s blank) following the assessment block was carried out in ascending order of spatial frequency. Within each pair. the order of stimulus presentation was determined by a quasi-random sequence (Fellows. 1967). After completion of the series of gratings and blanks, the test sequence including the “warm-up” block was then repeated. The total number of trials for training or testing sessions, including both warm-up blocks, was 336. In both the training and testing sessions, pecks on an incorrect key resulted in a 4.5 set period in which the keys and the chamber were dark and the shutter closed. Pecks on dark keys were ineffective. Following an error, a correction procedure was used in which the previous stimulus was repeated until the bird made the correct response. Error-correction responses were followed by the feeder light. but were never accompanied by the delivery of grain. During each session, the luminance of the center key was 1.0 cd/m2 or was attenuated by one, two or three of the OS neutral-density filters. The data from the first session at each level of target luminance were discarded. Testing was continued at different luminance levels (in quasi-random order) until data had been accumulated from three sessions at each luminance level. Prior to each session the birds were brought into the experimental room and placed in a ventilated cage draped with several layers of black felt cloth for I hr of dark adaptation. D. S. Blough (1956) has reported that the absolute threshold for target luminance reaches a minimum after approx 45 min of dark adaptation. In order to prevent the pigeons from falling asleep during dark adaptation we were obliged to enter the experimental room at 5-10 min intervals during the adaptation period and gently tap on the cage or move it slightly in order to maintain the birds in a state of wakefulness. RESI! LTS
The percentage of correct responses obtained with each stimulus pair was plotted as a function of the spatial frequency of the grating to form a psychometric function. The point of subjective equality was determined by the point at which the psychometric function crossed the 75% correct line, which is halfway between chance performance and perfect detection of the grating. The grating frequency at the point of subjective equality was taken to represent the minimum-separable spatial frequency. The visual-angle subtense of each grating bar at the point of subjective equality was estimated for each subject at each luminance level. In est~ating the angular subtense we assumed that the pigeons viewed the stimuli from the near-point of accommodation. I-Iodos et ul. (1976)
v -1.k
-1.b
-015
0.b
LUMINANCE (log
d.5 cd /m2 )
110
Fig. 1. Visual acuity of two pigeons as a function of target luminance under conditions of scotopic adaptation. Aiso shown is a portion of each pigeon’s photopic acuity-luminance function (Hodos et ai.. 1976).
estimated this distance to be 62 mm based on an analysis of 1000 frame/set motion picture films of pigeons viewing the stimuli in this apparatus and the schematic pigeon eye of ~arsh~1, Mellerio and Palmer (1973). Figure 1 indicates visual acuity (l/visual angle in min) as a function of target luminance. Also shown in the figure are the data of these two pigeons at comparable levels of target luminance under conditions of photopic adaptation (Hodos et ul., 1976). Pigeon C-412 showed a progressive decline in acuity at each successively lower target luminance. Acuity declined to 0.025 corresponding to a visual angle of 40’. Pigeon D-27 showed a lesser rate of decline than did C-412, but at the lowest luminance value, the two birds had nearly the same acuity. D-27’s acuity was 0.028, corresponding to a visual angle of 32’. Comparison of the scotopic and photopic acuity of the pigeons at roughly equal target luminances indicates that scotopic acuity is considerably poorer than photopic acuity. Photopic acuity at -0.07 log cd/m’ was 0.17-0.18, corresponding to visual angles of 5.8-5.6’, respectively. Scotopic acuity at 0.0 log cd/m’ was O.OY&U.Oll, corresponding to visual angles of 10.2-9.2’, respectively. DISCUSSION The psychometric functions indicated that only the 0.4 lines/mm grating could be reliably resolved by either subject at the lowest luminance used. The bar width of these gratings was 2.5 mm, with an angular subtense of 2.3”. At this frequency, only three bar/ space pairs were visible through the 1.5 cm aperture behind the glass center key. Indeed, a smaller number of bars may no longer constitute an adequate representation of a grating (Kelly, 1975; van den Brink and B&en, 1975). The results indicated that at roughly equivalent levels of target luminance (approx 1.Ocd/m2), the scotopically-adapted pigeon retina has approximately
465
Near-field visual acuity of pigeons
half the near-field visual acuity as the photopicallyadapted pigeon. However, since pigeons use different portions of the retina for near and far vision (Millodot and P. M. Blough, 1971; Nye, 1973) with different densities of receptors and ganglion cells (Binggeli and Paule, 1969; Galifret, 1966, 1968) the results might have been different had scotopic far-field acuity been measured in an apparatus similar to that used by P. M. Blough (1971, 1973). The luminance of the target at the rod-cone “break” of the pigeon dark-adaptation function (D. S. Blot@, 1956) was several log units below the “break” suggested by the present data. However, Blough’s experiment investigated the pigeon’s ability to detect a uniformly luminous field and not to resolve a spatial distribution of luminances within that field. The demands of the latter task are considerably greater. Figure 2 summarizes the currently available data on acuity-luminance functions for birds. Shown in the figure are data from pigeons based on the present report and Hodos et al. (1976), the great-horned owl, Bubo virginianus (Fite, 1973), the tawny owl, Strix aluco (Martin and Gordon, 1974), and the falcon, F&o sparverius (Fox et al., 1976). The figure indicates that the photopic acuity of pigeons exceeds that of the two owl species at comparable target luminances. A recent report by Fite et al. (1975) indicated that the upper limit of the acuity-luminance function of the northern blue-jay, Cyanocitta cristata, is similar to that of the pigeon; however, the blue-jays have somewhat higher acuity at the lower luminance levels. Both the tawny owl and pigeon functions show an abrupt fall-off of acuity at high luminances. Fite et al. (1975) reported a similar effect in blue jays. The decline in acuity at high target luminances may represent the effects of glare. -
““1 .2
0 So.
The inset figure indicates that at comparable targetluminance values, falcon acuity exceeds that of pigeons by a factor of about 10. Pigeons and greathorned owls have approximately equal acuity for grating targets with luminance of approx 1 cd/m’. However, the great-horned owl’s acuity is superior to the pigeon’s at lower target luminances under either condition of adaptation. An important consideration in comparing these acuity-luminance functions is that differences in retinal illumination have not been taken into account. If the abscissa represented retinal illumination rather than target luminance some displacement of the curves might have resulted. EXPERIMENT
2
The color vision of birds, particularly pigeons, has been extensively investigated in recent years. In addition to studies of both scotopic and photopic spectral sensitivity (D. S. Blough, 1957; Ikeda, 1965; P. M. Blough, Riggs and Schafer, 1972) investigations have been carried out of pigeons’ ability to discriminate small differences in wavelength and match wavelengths throughout the photopic spectrum (P. M. Blough, 1972; Wright, 1972; Wright and Cumming, 1971). Another series of studies explored possible underlying mechanism of avian color vision in terms of cone pigments and the colored oil droplets contained in the cones (Graf and van Norren, 1974; van Norren, 1975; Mayr, 1972; King-Smith, 1969; Pedler and Boyle, 1969, Sillman, 1969) and the spectral sensitivity of single neurons in the pigeon thalamus (Granda and Yazulla, 1971; Yazulla and Granda, 1973). However, no studies have investigated the visual acuity of birds in different regions of the photopic spectrum. The experiment reported here investigated the near-field visual acuity of pigeons with the illuminant confined to one of four relatively narrow bands of-the photopic spectrum. The results obtained were similar to data obtained from human observers.
045
METHOD
04D-
Subjects The subjects were the same as in experiment
0.35 3 p.30-
< ci f.
Y
1 42 0 F
0.2s 2 i 50.20-
5:
0.1%
0.1 o-
IO
0.05-
20 zcl 00
Fig. 2. Visual acuity of several species of birds as a function of target luminance.
1 with the addition of a third pigeon of similar age and experience in visual acuity experiments. Apparatus
The apparatus was the same as that reported in experiment 1, with the following modifications: (1) the grating stimuli ranged in spatial frequency from 2 to 24 lines/mm and in contrast from 98.9 to 93.7%. (2) During each experimental session, one of four narrow-pass, Kodak Wratten color filters was present in the beam path. Kodak Wratten No. 96, neutral-density filters were used to equate the chromatic filters for brightness based on heterochromatic brightness matches by pigeons reported by Hodos (1969). The Kodak Wratten filters that were used are listed below. The dominant wavelength of each filter and the optical density of the neutral density filter that was added to it are given in parentheses. No. 26 (619 nm + 1.0 n.d.); No. 73 (575 nm + 0.6 nd.); No. 93 (545 nm + 0.6 n.d.); No. 94 (458 nm + 0 n.d.). (3) The luminance of the stimulus field on the center key, with no filters in the beam path was 3.65 log cd/m2. (4) The overall chamber illumination was 171 lx and was
466
WILLIAM
HODOSand ROSAUNDW. LEIBOWITZ
produced by two ceiling-mounted, daylight, fluorescent lamps (General Electric F6T.5~CW-HH) diffused by a sheet of translucent plexiglass. (5) The chamber remained illuminated throughout the session. Procedure
The procedure was the same as in experiment 1. Prior to each session, one of the Wratten color filters was placed in the beam path: A different filter was used each day. The data collected during the first session with each filter were discarded. Testing was continued until data were collected from three sessions with each color filter. In order to obtain some data on human performance in this apparatus, which could be compared to the pigeons’ performance, two human subjects were tested. Each subject viewed the gratings through a 5 mm hole in the rear wall of the pigeon chamber. Their heads were maintained in position by a chin and forehead support frame. Push buttons were substituted for the keys and the feeder light provided feedback for correct responses. Each subject was tested for one session with each filter. The filters had been matched by the subjects for brightness by the addition of neutral density filters.
RESULTS Figure 3 presents the visual acuity (l/visual angle in min) of each pigeon as a function of the dominant
wavelength of the illuminant. In each case, peak acuity occurred when the 575 nm illuminant was used. These values ranged from 0.28 to 0.32, corresponding to visual angIes of 3.6-3.2’, respectively. Modest declines from these peak values were observed when the 619 and 545 nm illuminants were used. However, with the 458 nm illuminant, a sharp loss of acuity was observed. The acuity estimates of the subjects tested with this illuminant ranged from 0.076 to 0.090 corresponding to visual angles of 13.2-11.1: respectively. DISCUSSION
The results of this experiment pigeons had a peak acuity when nant was used. All three subjects of acuity at longer and shorter
indicated that the the 575 nm illumishowed a reduction wavelengths. These
3
0 30.
i
a. G 25Ir : 4 GZO4" 2 G 15; 0.10.
ii,
54% DOMINANT
.
v
c-412
-
c-580
c---L
D-27
5kD WAVELEtU3TH
six, (nm)
Fig. 3. Visual acuity of three pigeons as a function of the dominant wavelength of the illuminant.
460
500 WAVELENGTH
600
.
760
(nm)
Fig. 4. Acuity-wavelength functions of pigeons compared with similar functions obtained from two human subjects tested in the same apparatus and from the literature (Cavonius, 1967; Adrian, 1970).
data are roughly comparable in form to data obtained from human subjects in other laboratories, as well as from the human subjects in our laboratory tested with the pigeon apparatus. Figure 4 presents a comparison of the human and pigeon data. The data of Adrian (1970) are based on the detection of Landolt rings. Also shown in this section are the data from our two human subjects tested in the pigeon apparatus. The data from our human subjects are roughly similar to those reported by Cavonius (1967) for grating acuity. Those of the pigeons seem to be somewhat more comparable to those of Adrian (1970) for humans viewing Landolt rings. The similarity of human and pigeon spatial resolution at different wavelengths is surprising in view of the apparent differences in cone structure and photopigments (Graf and van Norren, 1974; van Norren. 1975, Mayr, 1972; King-Smith, 1969; Pedler and Boyle, 1969; Sillman, 1969). On the other hand, except for increased sensitivity to short wavelengths, pigeon and human photopic spectral sensitivity curves are quite similar (D. S. Blough, 1957: Ikeda, 1965; P. M. Blough et al., 1972). One of the principal differences between the avian and human retinas is the presence of colored oil droplets between the inner and outer segments of the majority of cones in the avian retinas (King-Smith, 1969; Pedler and Boyle, 1969; Mayr, 1972). The droplets are red, orange, yellow and colorless. The various droplets are not uniformly distributed throughout the retina. The region corresponding to the binocular field contains an exceptionafly high concentration of red and yellow droplets. This region has a reddish appearance in fresh preparation and is known as the red field. Since the binocular field is the field used for near vision (P. M. Blough, 1971, 1973; Catania, 1964; Millodot and Blough, 1971; Nye, 1973; Hodos et al., 1976) the high concentration of red and yellow droplets may have had an influence on the results. This could be tested by determining the effects of
Near-field visual acuity of pigeons wavelength on far-field acuity using a technique lar to that of P. M. Blough (1971, 1973).
simi-
Acknowledgements-The authors thank K. V. Fite, A. M. Granda and C. R. Cavonius for their valuable comments on the manuscript, S. Weiss and K. Macko who assisted in the collection of the human data, Janice Wilberger who prepared the manuscript for publication and the National Eye Institute, which supported this research through grant number EY-00735. REFERENCES
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