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Development of visual acuity in infant chimpanzees
INFANT
BEHAVIOR AND DEVELOPMENT
18,225-232
(1995)
Development of Visual Acuity in Infant Chimpanzees KIM
A. BARD, ELIZABETH A. STREET, CATHERINE MCCRARY, AND RONALD G. BOOTHE Yerkes Regional Primate Research Center, Atlanta
To assess development of visual acuity, a preferential looking procedure was administered to 13 nursery-reared chimpanzee infants ranging in age from 1 to 52 weeks. Chimpanzees exhibited acuity levels poorer than 1 cycle/degree when tested within the first weeks after birth, which is similar to that seen in neonatal humans and monkeys. Acuity improved about tenfold to near 10 cycles/degree during the first year. The time course of chimpanzee acuity development was more similar to that of humans than of monkeys. Tests were conducted at two or three separate viewing distances (38, 76, or 152 cm) in some individuals. This was done because previous observations during neurobehavioral assessments had found optimal focal distance to be longer in chimpanzee than in human infants. The results exhibited a nonsignificant trend for acuity to be better at far (76 or 152 cm) than at near (38 cm) viewing distances. These normative data can be usefully applied to further our understanding of the biological bases of perceptual and motor development and the effects of their coordination on subsequent development of other functions in primates. vision
great
ape
chimpanzee infant perceptual development
Studies of the vision of chimpanzee infants are important from several perspectives. Although there have been numerous investigations and assessments of visual function in infant monkeys and humans (Boothe, Dobson, & Teller, 1985), there have been only scattered reports of postnatal visual development in great apes. Furthermore, the studies that have been done are now several decades old and involved only a few subjects along the lines of case studies 1958b; Ordy, Latonick, (Fantz, 1958a, Samorajski, & Marsopust, 1964). More modem methods have been applied to larger populations of infant humans and monkeys in order to determine age norms. For example, modem behavioral studies have demonstrated similarities between Old World monkeys and humans
This study is the result of two student research projects conducted by E.A.S. and C.M. under the joint guidance of K.A.B. and R.G.B. The project was supported by NIH grant RR-00165 from the National Center for Research Resources to the Yerkes Primate Research Center, NIH grant RR-03591 to R. B. Swenson, and NIH grant RR06158 to K. A. B. The following research assistants provided invaluable assistance to this investigation: Lorissa Green, Marie Mize, Carolyn Fort, Jennifer Fineran, Paige McCurdy, Ben Jones, Carrie AM Rillo, Elizabeth Bell, Sheryl Williams, and Kathy Gardner. The Yerkes Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care. Correspondence and requests for reprints should be sent to Kim A. Bard, Yerkes Regional Primate Research Center, Emory University, Atlanta, GA 30322.
visual development
in the magnitude and progression of perceptual development of several visual functions, with the rate of development from birth approximately four times faster in monkeys than in humans (Boothe et al., 1985; Boothe, Kiorpes, Regal, & Lee, 1982; Gunderson & Swartz, 1985; Mendelson, 1982a, 1982b). A lack of data from our closer evolutionary relatives, the great apes, has hindered accurate analogous comparisons of rate of development between human and chimpanzee infants. There has been a recent upswing of interest in behavioral studies of chimpanzees (e.g., de Waal, 1989). A major aim of the current study was to contribute developmental information about visual acuity, a basic sensory capacity, to this expanding knowledge base regarding chimpanzees. Establishment of acuity age norms could be used for practical purposes such as to enable researchers to screen infant chimpanzees for visual deficits. Our interest in chimpanzees’ ability to attend to visual stimuli at varying distances was triggered by neonatal neurobehavioral tests (Bard, Platzman, Lester, & Suomi, 1992). Neonatal chimpanzees’ visual attention was most easily captured when stimuli were presented approximately 60 cm away rather than 25 cm, as preferred by human neonates. Studies of chimpanzees are also important from a perspective of developmental theories, most of which have been formulated on the basis of observations of only human children. 225
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Bard, Street, McCrary, and Boothe
Developmental theories often postulate specific mechanisms to allow development to progress from one level or stage to the next. An example would be the assertion that self-propelled locomotor exploration of the environment is necessary to allow a specific aspect of perceptual development to proceed (e.g., Bushnell & Boudreau, 1993). Sensory and motor development may not develop with the same time courses relative to one another in human and nonhuman primate infants (Vauclair, 1984). Thus, developmental studies with chimpanzees could provide direct tests of some theories or allow developmental factors that are confounded in human infants to be disentangled. A prerequisite for carrying out these kinds of studies is to have normative information available about basic motor and sensory capacities of infant chimpanzees. Studies that attempt to assess visual functions in nonverbal infants, both humans and nonhuman primates, share a number of methodological considerations. A variety of behavioral techniques have been developed over the years to assess the visual acuity in infant humans and monkeys, with some of the most successful involving preferential looking (Birch, 1989; Boothe, 1990; Dobson & Teller, 1978; Fantz, 1958a; Teller, 1979). Preferential looking procedures depend upon the fact that an infant, when presented with a high-contrast patterned target paired with a blank target of equal luminance, will look preferentially at the patterned target (Fantz, 1958a). Preferential looking methods allow perceptual functions to be measured in infant human and nonhuman primates with identical equipment and procedures (Boothe, 1990; Fantz, 1958a, 1958b; Teller, 1979, 1981). A number of recent modifications have been made to the basic preferential looking procedure in order to try to make the procedure more efficient or more rigorous in terms of its psychophysical rationale (Teller, 1979; Teller, McDonald, Preston, Sebris, & Dobson, 1986). The variation on this procedure which we used for this study is forced-choice preferential looking as adapted by Teller (1979). The goals of this study were (a) to establish age norms for acuity development in infant chimpanzees, (b) to compare these results to previously established findings in human and monkey infants, and (c) to compare acuity per-
formance by the chimpanzee viewing distances.
infants at different
METHOD Subjects and Longitudinal
Design
The subjects in this study were 13 infant chimpanzees (8 females, 5 males) placed in the Yerkes nursery due to inadequate maternal care (see Bard, 1994, 1995, and Bard et al., 1992, for more details concerning maternal competence and nursery care). Details about the individual subjects and their testing schedules are presented in Table I. The project initially began with 8 infant chimpanzees in the fall of 1990 and continued through April of 1991, it was then continued with 7 more infant chimpanzees in the fall of 1991 through December. Two of the infants used in the first round of testing, Artemus and Callie, were also retested during the second series of testing. Our overall age norms are based on a mixture of longitudinal and cross-sectional data, with each subject contributing repeated measures over a specific age range (see Table 1). The visual assessments were conducted by two different teams of testers, Team A for the first group (fall of 1990). and Team B for the second group (fall of 1991). We conducted a separate analysis to establish that the results obtained from these two separate tester teams were not significantly different. The infants tested by Team A were only tested at 38 and 76 cm due to technical limitations. Based on these preliminary results, Team B was able to collect additional data on some subjects at a viewing distance of 152 cm (see Table I).
Apparatus Stimuli consisted of a set of Teller Acuity Cards purchased from Vistech Consultants, Inc. (Dayton, OH). The set consisted of eight cards which displayed gratings (vertical black-and-white stripes) ranging in spatial frequency from 0.32 cycles/cm (the widest stripes) to 38.0 cycles/cm (the thinnest stripes). The grating occupied one side of the card, left or right, and the opposite side of the card was a homogeneous gray field. The space average luminance of the grating pattern on the card was matched to the homogeneous gray on the opposite side of the card to ensure that infant preference choices were based on pattern detection and not on differences in brightness. The cards were presented through a rectangular opening in a surrounding screen made of gray cardboard. This was done to minimize distractions from other activities taking place in the room during testing. A light meter was used to ensure that lighting in the testing area was sufficient to maintain luminance from the test cards at levels above 10 cd/m* (Brown, Dobson, & Maier, 1987). Lighting level remained constant throughout testing.
Preferential
Looking Procedure
A room in the Great Ape Nursery wing of the Yerkes Regional Primate Research Center was used for testing. All testing was carried out when the infant was in an alert but quiet state. Three human experimenters participated in testing. The infant chimpanzee was held in one experimenter’s lap (the holder) during testing. The holder attempted to
Chimpanzee
Acuity Development
TABLE 1 The Testing Schedule for Visual Acuity in Young Chimpanzees
Subject Name
Collie Evelyne Artemus Josh Lizzie Amanda Arthur Rebecca Zana Edwina Collie Bunny Eiwood Duff Artemus
Viewing Distances km1 38,76
38,76, 152 38,76 38,76 38,76 38,76,152 38,76, 152 38,76, 152 38,76 38,76, 152 38,76,152 38,76 38,76 38,76 38,76,152
Tester Team
e Range Af weeks)
A B A A A B B B A B B A A A B
l-7 2-10 6-14 1O-29 13-30 16-20 18-24 18-25 20-21 21-24 32-38 33-44 39-51 39-52 44
maintain infant comfort, alertness, and position. The holder sat facing the screen such that the infant’s eyes could bc positioned at a fixed distance (38.76, or 152 cm) in front of the grating card (Figure 1). Meanwhile, a second experimenter (the observer) observed the infant chimpanzee through a small peephole which was present in the center of each grating acuity card. The observer’s job was to make a judgment, based on the infant’s gaze pattern, about which side of the card contained the grating. The rationale for this procedure is based on the fact that infants prefer to look at stripes rather than homogeneous fields, and, thus, eye movements will allow the observer to figure out which side of the card has the grating if the infant can detect the grating. The observer was kept uninformed about which side of the card actually contained the grating until after the judgment had been made. Following each trial, the observer received feedback from the third experimenter about whether her judgment had been correct or wrong on that trial before proceeding to present the grating acuity card to the subject for the next trial. This feedback allowed observers to optimize performance by learning what idiosyncratic behaviors of each infant correlated with grating position. Occasionally, the roles of observer and third experimenter had to be performed by a single individual. In these cases, the cards were stacked face down in proper order of presentation, and the observer looked at the card following its presentation in order to receive feedback regarding correct judgment. The spatial frequencies of the grating acuity cards to be used were determined in advance of each test session and were based on the infants’ performance during the previous session. Before each testing session, the experimenter obtained a computer printout which listed five specific acuity cards to be used for that session along with a listing of the random order of presentation. The values of these five cards were determined by a computer program based on an algorithm that attempted to span the range of expected performance from near chance to near perfect.
227
The order of presentation of the live cards was determined by the psychophysical method of constant stimuli. Cards were presented in blocks of five within which each card was presented once, and both order of presentation and side of the card containing the grating were randomized within the block. Blocks of five were. then repeated in a new randomized order for as many repetitions as time and state of the subject allowed. At the end of each block of five, the experimenter made a judgment about whether or not the specific cards being used for that session were adequate and then made an adjustment either upward or downward for the following block as deemed appropriate. For example, if the observer made no mistakes on any of the five cards during a block, and all of the judgments seemed easy, then on the following block, the card with the lowest spatial frequency could be replaced with a new card having a spatial frequency one step higher than any currently being used. Data collected during a session had to be either accepted or rejected for further analysis in terms of these blocks of five. In other words, if the observer, experimenter, or holder determined that the state of the infant was such that testing should be stopped, then all data collected within the current block of five were eliminated, and only previously completed blocks within that session were subjected to further data analysis. In a typical session, five card blocks could be repeated to the subject for about eight replications before state variables or time constraints resulted in an end to the testing session. Blocks at different test distances were intermixed within a session with order of presentation counterbalanced across sessions. When the subject, the holder, the experimenter, and the observer were ready, the experimenter handed the observer the first randomized card and signaled the holder to look away from the screen. This was done to ensure that the holder did not bias the subject’s behavior based on her knowledge about which side of the card contained the grating. Then the observer placed the card up to the rectangular opening in the screen. The holder positioned the subject’s head at the proper location in front of the screen, and the observer watched for the subject’s response through the peephole at the center of the card. The observer observed the subject’s looking behavior and, on that basis, made a judgment about which side (left or right) contained the grating. The observer was allowed to take as much time as needed to make the judgment, but in practice, a trial was typically completed within a few seconds. During the time periods when a card was not being presented, the holder could interact with the infant to ensure continued interest and cooperation with the testing. To make an accurate assessment of the optimal focal distance in infant chimpanzees, tests were conducted at three fixed test distances (38, 76, and 152 cm) between the chimpanzee and the test card. The test distance was measured from the subject’s forehead to the peephole in the center of the test card.
Data Analysis It can be noted that the judgment of the observer in the particular variant of preferential looking we used is in regard to a physical state of the world (grating is on the left side of the card or on the right side of the card) which can be
Bard, Street, McCrary, and Boothe
228
Figure 1. An infant chimpanzee
during acuity testing with a forced-choice
labelled as correct or incorrect based on an external referent (Teller, 1979). Thus, the basic data are in the form of correct and incorrect trials which were accumulated by the observer for each chimpanzee for every condition that was tested. We transformed the physical spatial frequency of the grating on each card (cycles/cm) into a viewer-centered value by calculating the cycles/degree subtended at the eye of the subject. Then we tabulated the number of correct and incorrect responses at each cycles/degree condition that was tested during a single session. There were typically not enough data collected during a single session to make a meaningful comparison between conditions, so the next step was to combine the results from one or more sessions into an age bin. The results of each chimpanzee were grouped into octave age bins which were centered around 2 (1.&2.8), 4 (2.8-5.6). 8 (5.6-l 1.3), 16 (11.3-22.6), and 32 (22.H5.2) weeks of age. Note that data for ages less than 1.4 weeks and greater than 45.2 were ignored in order to avoid skewing the distribution of ages within each octave bin. The reason for grouping into logarithmic instead of linear age bins is because the appropriate metric for specifying acuity is logarithmic (Westheimer, 1979), and log acuity improves according to a nonlinear growth function. As a first order approximation, octave age bins group data such that each successive age bin reflects a similar magnitude of improvement (Boothe, 1990; see also Figure 2 of this article). We used probit analysis (Finney, 1971) to fit a psychometric function at each age bin for each condition tested for each subject. The form of these psychometric functions is illustrated in Figure 2. Acuity was then derived from the psychometric function as the spatial frequency in cycles/degree where the function intersected 75% correct. Finally, in order to illustrate group results, we calculated the mean and standard error of acuity values across individual chimpanzees within each age bin. We used logarithms of the individual acuity values when calculating the mean (Westheimer, 1979). No individual subject contributed more than one value to any single age bin, but most subjects contributed a value to more than one age bin. Separate acuity
preferential
looking procedure.
estimates were also derived, as just described, viewing distance tested within each age bin.
for each
RESULTS Figures 2a through e illustrate the raw data and derived psychometric function for a representative subject in each age bin. The percentage of correct responses at each spatial frequency tested are shown by the star symbols, and the smooth curve is the best fitting probit. Examination of these raw data sets, as illustrated in Figure 2, strengthened our confidence in the face validity of the final acuity estimates. The fact that performance falls to near chance at higher spatial frequencies allows us to rule out a number of potential methodological artifacts. Similarly, the fact that performance improves to substantially better than chance at lower spatial frequencies demonstrates that behavior is under stimulus control. The spatial frequency (in cycles/degree) where each smooth curve shown in Figure 2 intersects 75% correct (designated with a plus symbol) is taken as the acuity estimate for this subject at this age. Similar analysis was done for each individual subject at each age tested. Results from individual subjects were then combined (as described in the Method section) to arrive at a group estimate of acuity within each age bin. Because the data were obtained from two separate test teams, we conducted an initial statistical comparison of the results from the two teams. There were two age bins with enough data from each
Chimpanzee
Acuity
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Bard, Street, McCrary, and Boothe DEVELOPMENT
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age in weeks Figure 3. Mean values of chimpanzee visual acuity at each age bin are shown by the asterisk symbols. Error bars show between-subiects standard errors around the means. (The exception is the data int at 4 weeks which is based on only 1 subject, EveV ne.) The upper and lower dashed lines represent the approximate acuity values expected for infant monkey and human subiects, respectively.
team to do a comparison. At 16 weeks, the results obtained from the two teams were not significantly different, t(5) = 2.36, p = .06.5. Similarly the results were not significantly different at 32 weeks, t(8) = 0.58, p = .576. Thus, we combined the results obtained from the two test teams; these results are shown graphically in Figure 3. Examination of this figure reveals that acuity starts out poorer than 1 cycle/degree shortly after birth and improves about tenfold to near 10 cycles/degree by the 32-week age bin. The dashed lines in Figure 3 illustrate the development of acuity that would be expected for infant monkeys (upper dashed line) and humans (lower dashed line). Most error bars overlap with the human but not with the monkey dashed line, demonstrating that acuity development in chimpanzees is more similar to that of humans than monkeys. The group data shown in Figure 3 exhibit an approximately constant improvement in acuity at a rate of about 0.25 cycles/degree per week. However, we cannot conclude from these results alone that individual chimpanzees will show this same rate of development, because the group means are based on a combination of repeated measures and cross-sectional data. To address this question, we calculated the average rate of improvement for every individual subject where we had acuity estimates at two dif-
ferent ages by dividing the difference in acuity at the two ages by the separation of the measurements in weeks. In cases where we had three or more measures from an individual, we took the average of the results from the individual pairs. The average rate of improvement in cycles/degree per week shown by the individual subjects was similar to that of the group, and the standard error of the mean of the individual subjects overlapped with the group mean (.32 f .07). We conclude that the rate of development depicted in Figure 3 applies to individual subjects as well as to the group. In order to assess optimal focal distances for infant chimpanzees, we also made a comparison of the acuity results obtained at different distances. A log difference score was obtained for each subject that had been tested at both 38 and 76 cm within a given age bin by subtracting the log acuity obtained at 76 cm from the log acuity obtained at 38 cm. The results were in the proper direction within each age bin to suggest that acuity is better at 76 cm than at 38 cm. However, a statistical test revealed that the differences were not significantly different from zero, t( 13) = 1.74, p = .l 1. We also performed separate tests at only the younger age bins to determine whether there was a significant difference at the young ages that failed to reach significance only because it went away at older ages. However, none of the tests reached statistical significance. A similar analysis was done comparing the smaller subset of results obtained at 152 cm with those at 38 cm. These results were also consistently in the proper direction to suggest that acuity at 152 cm was better than at 38 cm. However, these differences also failed to reach statistical significance, r(5) = 1.47, p = .201. DISCUSSION The results of several previous studies of acuity development in humans and in macaque monkeys have demonstrated that acuity develops about four times faster in monkeys than in humans (Boothe et al., 1985). This has led to the formulation of the general principle that acuity development in monkeys in weeks is similar to acuity development in humans in months. The absolute acuity values as a function of age can be conveniently remembered by noting that acuity specified in grating cycles per degree is approximately equal to age (in
Chimpanzee
231
Acuity Development
weeks in monkeys and in months in humans). Chimpanzees are more similar to humans than to monkeys in this regard as demonstrated by the dashed lines shown in Figure 3 which represent the expected acuity values for humans (bottom) and monkeys (top). The standard error bars of the chimpanzees are near, or overlap, with the time course expected for humans but are separated further from, and do not overlap with, the time course expected for monkeys. The visual system is not mature at 1 year of age in humans, and acuity only begins to asymptote near adult levels of 30 to 50 cycles/degree at 3 to 5 years. Further research is needed to determine the comparable age for chimpanzees, but based on the similarities seen over the first year, and on their comparable life spans, we would expect acuity to also continue to improve for the first 3 to 5 years in chimpanzees. Our previous observations of preferred focal distances during neurobehavioral testing revealed stronger responses for distant targets (Bard et al., 1992). A human examiner holds human infants at a distance of 25 cm and chimpanzee infants at a distance of 60 cm in order to assess orientation to the face. There may be a difference in the visual systems of neonatal humans and chimpanzees in this regard. It is difficult to determine if acuity or accommodation is responsible for the observation that human neonates tend to prefer to fixate objects at about 25 cm, although under appropriate circumstances they appear able to accommodate to more distant objects as well (Aslin & Jackson, 1979; Banks, 1980; Braddick, Atkinson, French, & Howland, 1979; Brookman, 1983; Haynes, White, & Held, 1965; McKenzie & Day, 1972). Our results are in the right direction to suggest a potential explanation for the preferences of the infant chimpanzees. Perhaps the preferences reflect the simple fact that they can see better at far distances than at near distances. Unfortunately, our results failed to reach statistical significance and will have to be repeated with a larger number of subjects in order to test this hypothesis. Previous studies suggest that chimpanzees develop biobehaviorally more rapidly than humans and may also be slightly more mature at birth than humans (Bard et al., 1992). This allows for the potential to use the chimpanzee to test developmental theories that have been formulated on the basis of observations only on
humans. If the chimpanzee infant is at a different relative level of maturation than the human, comparative studies with the human and chimpanzee may allow one to disentangle which factors are responsible for developmental progression to the next stage. This comparative developmental perspective may allow specific hypotheses to be tested (i.e., falsified) in a manner that would be impossible through the singular study of human infants. This can be illustrated by a specific example. There has been a recent emphasis on blending an ecological and a dynamic approach to development (Gibson, 1982; Lockman & Thelen, 1993). Thus, the focus has changed from fixed age-linked milestones to developmental transitions. The age of onset of the transition to independent locomotion, for instance, dramatically changes the infant’s relation to his or her environment and may have repercussions on social dynamics, including temperament, as well as perceptual processing (Campos, 1992; Emde, Jones, & Henderson, 1992). Chimpanzee infants begin crawling earlier than humans at around 4 months of age (Veira & Bard, 1994; Riesen & Kinder, 1952) which is about the same time they begin to be successful in reaching and grasping for objects (Bard, Gardner, & Platzman, 1991). Chimpanzees’ relatively rapid motor development but relatively more similar visual development compared with human infants could be used to further investigate causal factors regulating relationships between the motor and perceptual systems during early infancy and the repercussions of these relationships on other aspects of development. REFERENCES Aslin,
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In W.A. Collins (Ed.), Minnesota S?~mposra on Child Psychology (Vol. 15). Hillsdale, NJ: Erlbaum. Gunderson, V.M., & Swartz, K.B. (1985). Visual recognition in infant pigtailed macaques after a 24.hour delay. American Journal of PrimatoloLqv, X.259-264. Haynes, H., White, B., & Held, R. (1965). Visual accommodation in human infants. Science. 148, 528-530. Lockman, J.J., & Thelen, E. (1993). Developmental biodynamics: Brain, body, behavior connections. Child Development. 64,953-959. McKenzie, B.E., & Day, R.H. (1972). Object distance as a determinant of visual fixation in early infancy. Science, 17X, 1108-I 110. Mendelson, M.J. (1982a). Clinical examination of visual and social responses in infant rhesus monkeys. Developmental Psychology, 18, 658-662. Mendelson, M.J. (1982b). Visual and social responses in infant rhesus monkeys. American Journal ofPrimatology, 3,333-340. Ordy, J.M., Latonick, A., Samorajski, T.. & Maraopust. L.C. (1964). Visual acuity in newborn primate infants. Proceedings ofthe Society for Experimental Biology and Medicine, 115, 677-680. Riesen, A.H., & Kinder, E.F. (1952). Postural development of infant chimpanzees. New Haven. CT: Yale University Press. Teller, D.Y. (1979). The forced-choice preferential looking procedure: A psychophysical technique for use with human infants. Infant Behavior and Development, 2. 135-153. Teller, D.Y. (1981). The development of visual acuity in human and monkey infants. Trends rn Neuroscience, 4, 21-24. Teller, D.Y., McDonald, M.A., Preston, K., Sebris, S.L., & Dobson, V. (1986). Assessment of visual acuity in infants and children: The acuity card procedure. Developmental Medir,ine and Child Neurology. 28. 779-789. Vauclair, J. (1984). Phylogenetic approach to object matupulation in human and ape infants. Human Development, 27, 32 I-32X. Veira, Y.. & Bard, K.A., (1994). Developmental milestones for chimpanzees raised in a responsive care nursery. American Journal of Primatolqy, 33. 246. Waal, F. de (198’)). Peacemakiqq among primates Cambridge, MA: Harvard University Press. Westheimer, G. (1979). Scaling of visual acuity measurements. Archi1,e.s ofOphthalmolo,~y, 97. 327-330.
05 February
1994;
Revised 24 May 1994
n
BEHAVIOR AND DEVELOPMENT
18,225-232
(1995)
Development of Visual Acuity in Infant Chimpanzees KIM
A. BARD, ELIZABETH A. STREET, CATHERINE MCCRARY, AND RONALD G. BOOTHE Yerkes Regional Primate Research Center, Atlanta
To assess development of visual acuity, a preferential looking procedure was administered to 13 nursery-reared chimpanzee infants ranging in age from 1 to 52 weeks. Chimpanzees exhibited acuity levels poorer than 1 cycle/degree when tested within the first weeks after birth, which is similar to that seen in neonatal humans and monkeys. Acuity improved about tenfold to near 10 cycles/degree during the first year. The time course of chimpanzee acuity development was more similar to that of humans than of monkeys. Tests were conducted at two or three separate viewing distances (38, 76, or 152 cm) in some individuals. This was done because previous observations during neurobehavioral assessments had found optimal focal distance to be longer in chimpanzee than in human infants. The results exhibited a nonsignificant trend for acuity to be better at far (76 or 152 cm) than at near (38 cm) viewing distances. These normative data can be usefully applied to further our understanding of the biological bases of perceptual and motor development and the effects of their coordination on subsequent development of other functions in primates. vision
great
ape
chimpanzee infant perceptual development
Studies of the vision of chimpanzee infants are important from several perspectives. Although there have been numerous investigations and assessments of visual function in infant monkeys and humans (Boothe, Dobson, & Teller, 1985), there have been only scattered reports of postnatal visual development in great apes. Furthermore, the studies that have been done are now several decades old and involved only a few subjects along the lines of case studies 1958b; Ordy, Latonick, (Fantz, 1958a, Samorajski, & Marsopust, 1964). More modem methods have been applied to larger populations of infant humans and monkeys in order to determine age norms. For example, modem behavioral studies have demonstrated similarities between Old World monkeys and humans
This study is the result of two student research projects conducted by E.A.S. and C.M. under the joint guidance of K.A.B. and R.G.B. The project was supported by NIH grant RR-00165 from the National Center for Research Resources to the Yerkes Primate Research Center, NIH grant RR-03591 to R. B. Swenson, and NIH grant RR06158 to K. A. B. The following research assistants provided invaluable assistance to this investigation: Lorissa Green, Marie Mize, Carolyn Fort, Jennifer Fineran, Paige McCurdy, Ben Jones, Carrie AM Rillo, Elizabeth Bell, Sheryl Williams, and Kathy Gardner. The Yerkes Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care. Correspondence and requests for reprints should be sent to Kim A. Bard, Yerkes Regional Primate Research Center, Emory University, Atlanta, GA 30322.
visual development
in the magnitude and progression of perceptual development of several visual functions, with the rate of development from birth approximately four times faster in monkeys than in humans (Boothe et al., 1985; Boothe, Kiorpes, Regal, & Lee, 1982; Gunderson & Swartz, 1985; Mendelson, 1982a, 1982b). A lack of data from our closer evolutionary relatives, the great apes, has hindered accurate analogous comparisons of rate of development between human and chimpanzee infants. There has been a recent upswing of interest in behavioral studies of chimpanzees (e.g., de Waal, 1989). A major aim of the current study was to contribute developmental information about visual acuity, a basic sensory capacity, to this expanding knowledge base regarding chimpanzees. Establishment of acuity age norms could be used for practical purposes such as to enable researchers to screen infant chimpanzees for visual deficits. Our interest in chimpanzees’ ability to attend to visual stimuli at varying distances was triggered by neonatal neurobehavioral tests (Bard, Platzman, Lester, & Suomi, 1992). Neonatal chimpanzees’ visual attention was most easily captured when stimuli were presented approximately 60 cm away rather than 25 cm, as preferred by human neonates. Studies of chimpanzees are also important from a perspective of developmental theories, most of which have been formulated on the basis of observations of only human children. 225
226
Bard, Street, McCrary, and Boothe
Developmental theories often postulate specific mechanisms to allow development to progress from one level or stage to the next. An example would be the assertion that self-propelled locomotor exploration of the environment is necessary to allow a specific aspect of perceptual development to proceed (e.g., Bushnell & Boudreau, 1993). Sensory and motor development may not develop with the same time courses relative to one another in human and nonhuman primate infants (Vauclair, 1984). Thus, developmental studies with chimpanzees could provide direct tests of some theories or allow developmental factors that are confounded in human infants to be disentangled. A prerequisite for carrying out these kinds of studies is to have normative information available about basic motor and sensory capacities of infant chimpanzees. Studies that attempt to assess visual functions in nonverbal infants, both humans and nonhuman primates, share a number of methodological considerations. A variety of behavioral techniques have been developed over the years to assess the visual acuity in infant humans and monkeys, with some of the most successful involving preferential looking (Birch, 1989; Boothe, 1990; Dobson & Teller, 1978; Fantz, 1958a; Teller, 1979). Preferential looking procedures depend upon the fact that an infant, when presented with a high-contrast patterned target paired with a blank target of equal luminance, will look preferentially at the patterned target (Fantz, 1958a). Preferential looking methods allow perceptual functions to be measured in infant human and nonhuman primates with identical equipment and procedures (Boothe, 1990; Fantz, 1958a, 1958b; Teller, 1979, 1981). A number of recent modifications have been made to the basic preferential looking procedure in order to try to make the procedure more efficient or more rigorous in terms of its psychophysical rationale (Teller, 1979; Teller, McDonald, Preston, Sebris, & Dobson, 1986). The variation on this procedure which we used for this study is forced-choice preferential looking as adapted by Teller (1979). The goals of this study were (a) to establish age norms for acuity development in infant chimpanzees, (b) to compare these results to previously established findings in human and monkey infants, and (c) to compare acuity per-
formance by the chimpanzee viewing distances.
infants at different
METHOD Subjects and Longitudinal
Design
The subjects in this study were 13 infant chimpanzees (8 females, 5 males) placed in the Yerkes nursery due to inadequate maternal care (see Bard, 1994, 1995, and Bard et al., 1992, for more details concerning maternal competence and nursery care). Details about the individual subjects and their testing schedules are presented in Table I. The project initially began with 8 infant chimpanzees in the fall of 1990 and continued through April of 1991, it was then continued with 7 more infant chimpanzees in the fall of 1991 through December. Two of the infants used in the first round of testing, Artemus and Callie, were also retested during the second series of testing. Our overall age norms are based on a mixture of longitudinal and cross-sectional data, with each subject contributing repeated measures over a specific age range (see Table 1). The visual assessments were conducted by two different teams of testers, Team A for the first group (fall of 1990). and Team B for the second group (fall of 1991). We conducted a separate analysis to establish that the results obtained from these two separate tester teams were not significantly different. The infants tested by Team A were only tested at 38 and 76 cm due to technical limitations. Based on these preliminary results, Team B was able to collect additional data on some subjects at a viewing distance of 152 cm (see Table I).
Apparatus Stimuli consisted of a set of Teller Acuity Cards purchased from Vistech Consultants, Inc. (Dayton, OH). The set consisted of eight cards which displayed gratings (vertical black-and-white stripes) ranging in spatial frequency from 0.32 cycles/cm (the widest stripes) to 38.0 cycles/cm (the thinnest stripes). The grating occupied one side of the card, left or right, and the opposite side of the card was a homogeneous gray field. The space average luminance of the grating pattern on the card was matched to the homogeneous gray on the opposite side of the card to ensure that infant preference choices were based on pattern detection and not on differences in brightness. The cards were presented through a rectangular opening in a surrounding screen made of gray cardboard. This was done to minimize distractions from other activities taking place in the room during testing. A light meter was used to ensure that lighting in the testing area was sufficient to maintain luminance from the test cards at levels above 10 cd/m* (Brown, Dobson, & Maier, 1987). Lighting level remained constant throughout testing.
Preferential
Looking Procedure
A room in the Great Ape Nursery wing of the Yerkes Regional Primate Research Center was used for testing. All testing was carried out when the infant was in an alert but quiet state. Three human experimenters participated in testing. The infant chimpanzee was held in one experimenter’s lap (the holder) during testing. The holder attempted to
Chimpanzee
Acuity Development
TABLE 1 The Testing Schedule for Visual Acuity in Young Chimpanzees
Subject Name
Collie Evelyne Artemus Josh Lizzie Amanda Arthur Rebecca Zana Edwina Collie Bunny Eiwood Duff Artemus
Viewing Distances km1 38,76
38,76, 152 38,76 38,76 38,76 38,76,152 38,76, 152 38,76, 152 38,76 38,76, 152 38,76,152 38,76 38,76 38,76 38,76,152
Tester Team
e Range Af weeks)
A B A A A B B B A B B A A A B
l-7 2-10 6-14 1O-29 13-30 16-20 18-24 18-25 20-21 21-24 32-38 33-44 39-51 39-52 44
maintain infant comfort, alertness, and position. The holder sat facing the screen such that the infant’s eyes could bc positioned at a fixed distance (38.76, or 152 cm) in front of the grating card (Figure 1). Meanwhile, a second experimenter (the observer) observed the infant chimpanzee through a small peephole which was present in the center of each grating acuity card. The observer’s job was to make a judgment, based on the infant’s gaze pattern, about which side of the card contained the grating. The rationale for this procedure is based on the fact that infants prefer to look at stripes rather than homogeneous fields, and, thus, eye movements will allow the observer to figure out which side of the card has the grating if the infant can detect the grating. The observer was kept uninformed about which side of the card actually contained the grating until after the judgment had been made. Following each trial, the observer received feedback from the third experimenter about whether her judgment had been correct or wrong on that trial before proceeding to present the grating acuity card to the subject for the next trial. This feedback allowed observers to optimize performance by learning what idiosyncratic behaviors of each infant correlated with grating position. Occasionally, the roles of observer and third experimenter had to be performed by a single individual. In these cases, the cards were stacked face down in proper order of presentation, and the observer looked at the card following its presentation in order to receive feedback regarding correct judgment. The spatial frequencies of the grating acuity cards to be used were determined in advance of each test session and were based on the infants’ performance during the previous session. Before each testing session, the experimenter obtained a computer printout which listed five specific acuity cards to be used for that session along with a listing of the random order of presentation. The values of these five cards were determined by a computer program based on an algorithm that attempted to span the range of expected performance from near chance to near perfect.
227
The order of presentation of the live cards was determined by the psychophysical method of constant stimuli. Cards were presented in blocks of five within which each card was presented once, and both order of presentation and side of the card containing the grating were randomized within the block. Blocks of five were. then repeated in a new randomized order for as many repetitions as time and state of the subject allowed. At the end of each block of five, the experimenter made a judgment about whether or not the specific cards being used for that session were adequate and then made an adjustment either upward or downward for the following block as deemed appropriate. For example, if the observer made no mistakes on any of the five cards during a block, and all of the judgments seemed easy, then on the following block, the card with the lowest spatial frequency could be replaced with a new card having a spatial frequency one step higher than any currently being used. Data collected during a session had to be either accepted or rejected for further analysis in terms of these blocks of five. In other words, if the observer, experimenter, or holder determined that the state of the infant was such that testing should be stopped, then all data collected within the current block of five were eliminated, and only previously completed blocks within that session were subjected to further data analysis. In a typical session, five card blocks could be repeated to the subject for about eight replications before state variables or time constraints resulted in an end to the testing session. Blocks at different test distances were intermixed within a session with order of presentation counterbalanced across sessions. When the subject, the holder, the experimenter, and the observer were ready, the experimenter handed the observer the first randomized card and signaled the holder to look away from the screen. This was done to ensure that the holder did not bias the subject’s behavior based on her knowledge about which side of the card contained the grating. Then the observer placed the card up to the rectangular opening in the screen. The holder positioned the subject’s head at the proper location in front of the screen, and the observer watched for the subject’s response through the peephole at the center of the card. The observer observed the subject’s looking behavior and, on that basis, made a judgment about which side (left or right) contained the grating. The observer was allowed to take as much time as needed to make the judgment, but in practice, a trial was typically completed within a few seconds. During the time periods when a card was not being presented, the holder could interact with the infant to ensure continued interest and cooperation with the testing. To make an accurate assessment of the optimal focal distance in infant chimpanzees, tests were conducted at three fixed test distances (38, 76, and 152 cm) between the chimpanzee and the test card. The test distance was measured from the subject’s forehead to the peephole in the center of the test card.
Data Analysis It can be noted that the judgment of the observer in the particular variant of preferential looking we used is in regard to a physical state of the world (grating is on the left side of the card or on the right side of the card) which can be
Bard, Street, McCrary, and Boothe
228
Figure 1. An infant chimpanzee
during acuity testing with a forced-choice
labelled as correct or incorrect based on an external referent (Teller, 1979). Thus, the basic data are in the form of correct and incorrect trials which were accumulated by the observer for each chimpanzee for every condition that was tested. We transformed the physical spatial frequency of the grating on each card (cycles/cm) into a viewer-centered value by calculating the cycles/degree subtended at the eye of the subject. Then we tabulated the number of correct and incorrect responses at each cycles/degree condition that was tested during a single session. There were typically not enough data collected during a single session to make a meaningful comparison between conditions, so the next step was to combine the results from one or more sessions into an age bin. The results of each chimpanzee were grouped into octave age bins which were centered around 2 (1.&2.8), 4 (2.8-5.6). 8 (5.6-l 1.3), 16 (11.3-22.6), and 32 (22.H5.2) weeks of age. Note that data for ages less than 1.4 weeks and greater than 45.2 were ignored in order to avoid skewing the distribution of ages within each octave bin. The reason for grouping into logarithmic instead of linear age bins is because the appropriate metric for specifying acuity is logarithmic (Westheimer, 1979), and log acuity improves according to a nonlinear growth function. As a first order approximation, octave age bins group data such that each successive age bin reflects a similar magnitude of improvement (Boothe, 1990; see also Figure 2 of this article). We used probit analysis (Finney, 1971) to fit a psychometric function at each age bin for each condition tested for each subject. The form of these psychometric functions is illustrated in Figure 2. Acuity was then derived from the psychometric function as the spatial frequency in cycles/degree where the function intersected 75% correct. Finally, in order to illustrate group results, we calculated the mean and standard error of acuity values across individual chimpanzees within each age bin. We used logarithms of the individual acuity values when calculating the mean (Westheimer, 1979). No individual subject contributed more than one value to any single age bin, but most subjects contributed a value to more than one age bin. Separate acuity
preferential
looking procedure.
estimates were also derived, as just described, viewing distance tested within each age bin.
for each
RESULTS Figures 2a through e illustrate the raw data and derived psychometric function for a representative subject in each age bin. The percentage of correct responses at each spatial frequency tested are shown by the star symbols, and the smooth curve is the best fitting probit. Examination of these raw data sets, as illustrated in Figure 2, strengthened our confidence in the face validity of the final acuity estimates. The fact that performance falls to near chance at higher spatial frequencies allows us to rule out a number of potential methodological artifacts. Similarly, the fact that performance improves to substantially better than chance at lower spatial frequencies demonstrates that behavior is under stimulus control. The spatial frequency (in cycles/degree) where each smooth curve shown in Figure 2 intersects 75% correct (designated with a plus symbol) is taken as the acuity estimate for this subject at this age. Similar analysis was done for each individual subject at each age tested. Results from individual subjects were then combined (as described in the Method section) to arrive at a group estimate of acuity within each age bin. Because the data were obtained from two separate test teams, we conducted an initial statistical comparison of the results from the two teams. There were two age bins with enough data from each
Chimpanzee
Acuity
Development
PsychometricFunction Fit By Profit Evelyne at 2 weeks
229
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230
Bard, Street, McCrary, and Boothe DEVELOPMENT
OF GRATING ACUITY
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age in weeks Figure 3. Mean values of chimpanzee visual acuity at each age bin are shown by the asterisk symbols. Error bars show between-subiects standard errors around the means. (The exception is the data int at 4 weeks which is based on only 1 subject, EveV ne.) The upper and lower dashed lines represent the approximate acuity values expected for infant monkey and human subiects, respectively.
team to do a comparison. At 16 weeks, the results obtained from the two teams were not significantly different, t(5) = 2.36, p = .06.5. Similarly the results were not significantly different at 32 weeks, t(8) = 0.58, p = .576. Thus, we combined the results obtained from the two test teams; these results are shown graphically in Figure 3. Examination of this figure reveals that acuity starts out poorer than 1 cycle/degree shortly after birth and improves about tenfold to near 10 cycles/degree by the 32-week age bin. The dashed lines in Figure 3 illustrate the development of acuity that would be expected for infant monkeys (upper dashed line) and humans (lower dashed line). Most error bars overlap with the human but not with the monkey dashed line, demonstrating that acuity development in chimpanzees is more similar to that of humans than monkeys. The group data shown in Figure 3 exhibit an approximately constant improvement in acuity at a rate of about 0.25 cycles/degree per week. However, we cannot conclude from these results alone that individual chimpanzees will show this same rate of development, because the group means are based on a combination of repeated measures and cross-sectional data. To address this question, we calculated the average rate of improvement for every individual subject where we had acuity estimates at two dif-
ferent ages by dividing the difference in acuity at the two ages by the separation of the measurements in weeks. In cases where we had three or more measures from an individual, we took the average of the results from the individual pairs. The average rate of improvement in cycles/degree per week shown by the individual subjects was similar to that of the group, and the standard error of the mean of the individual subjects overlapped with the group mean (.32 f .07). We conclude that the rate of development depicted in Figure 3 applies to individual subjects as well as to the group. In order to assess optimal focal distances for infant chimpanzees, we also made a comparison of the acuity results obtained at different distances. A log difference score was obtained for each subject that had been tested at both 38 and 76 cm within a given age bin by subtracting the log acuity obtained at 76 cm from the log acuity obtained at 38 cm. The results were in the proper direction within each age bin to suggest that acuity is better at 76 cm than at 38 cm. However, a statistical test revealed that the differences were not significantly different from zero, t( 13) = 1.74, p = .l 1. We also performed separate tests at only the younger age bins to determine whether there was a significant difference at the young ages that failed to reach significance only because it went away at older ages. However, none of the tests reached statistical significance. A similar analysis was done comparing the smaller subset of results obtained at 152 cm with those at 38 cm. These results were also consistently in the proper direction to suggest that acuity at 152 cm was better than at 38 cm. However, these differences also failed to reach statistical significance, r(5) = 1.47, p = .201. DISCUSSION The results of several previous studies of acuity development in humans and in macaque monkeys have demonstrated that acuity develops about four times faster in monkeys than in humans (Boothe et al., 1985). This has led to the formulation of the general principle that acuity development in monkeys in weeks is similar to acuity development in humans in months. The absolute acuity values as a function of age can be conveniently remembered by noting that acuity specified in grating cycles per degree is approximately equal to age (in
Chimpanzee
231
Acuity Development
weeks in monkeys and in months in humans). Chimpanzees are more similar to humans than to monkeys in this regard as demonstrated by the dashed lines shown in Figure 3 which represent the expected acuity values for humans (bottom) and monkeys (top). The standard error bars of the chimpanzees are near, or overlap, with the time course expected for humans but are separated further from, and do not overlap with, the time course expected for monkeys. The visual system is not mature at 1 year of age in humans, and acuity only begins to asymptote near adult levels of 30 to 50 cycles/degree at 3 to 5 years. Further research is needed to determine the comparable age for chimpanzees, but based on the similarities seen over the first year, and on their comparable life spans, we would expect acuity to also continue to improve for the first 3 to 5 years in chimpanzees. Our previous observations of preferred focal distances during neurobehavioral testing revealed stronger responses for distant targets (Bard et al., 1992). A human examiner holds human infants at a distance of 25 cm and chimpanzee infants at a distance of 60 cm in order to assess orientation to the face. There may be a difference in the visual systems of neonatal humans and chimpanzees in this regard. It is difficult to determine if acuity or accommodation is responsible for the observation that human neonates tend to prefer to fixate objects at about 25 cm, although under appropriate circumstances they appear able to accommodate to more distant objects as well (Aslin & Jackson, 1979; Banks, 1980; Braddick, Atkinson, French, & Howland, 1979; Brookman, 1983; Haynes, White, & Held, 1965; McKenzie & Day, 1972). Our results are in the right direction to suggest a potential explanation for the preferences of the infant chimpanzees. Perhaps the preferences reflect the simple fact that they can see better at far distances than at near distances. Unfortunately, our results failed to reach statistical significance and will have to be repeated with a larger number of subjects in order to test this hypothesis. Previous studies suggest that chimpanzees develop biobehaviorally more rapidly than humans and may also be slightly more mature at birth than humans (Bard et al., 1992). This allows for the potential to use the chimpanzee to test developmental theories that have been formulated on the basis of observations only on
humans. If the chimpanzee infant is at a different relative level of maturation than the human, comparative studies with the human and chimpanzee may allow one to disentangle which factors are responsible for developmental progression to the next stage. This comparative developmental perspective may allow specific hypotheses to be tested (i.e., falsified) in a manner that would be impossible through the singular study of human infants. This can be illustrated by a specific example. There has been a recent emphasis on blending an ecological and a dynamic approach to development (Gibson, 1982; Lockman & Thelen, 1993). Thus, the focus has changed from fixed age-linked milestones to developmental transitions. The age of onset of the transition to independent locomotion, for instance, dramatically changes the infant’s relation to his or her environment and may have repercussions on social dynamics, including temperament, as well as perceptual processing (Campos, 1992; Emde, Jones, & Henderson, 1992). Chimpanzee infants begin crawling earlier than humans at around 4 months of age (Veira & Bard, 1994; Riesen & Kinder, 1952) which is about the same time they begin to be successful in reaching and grasping for objects (Bard, Gardner, & Platzman, 1991). Chimpanzees’ relatively rapid motor development but relatively more similar visual development compared with human infants could be used to further investigate causal factors regulating relationships between the motor and perceptual systems during early infancy and the repercussions of these relationships on other aspects of development. REFERENCES Aslin,
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