Visually normal adults experience a world composed of objects that endure in space and time even when those objects are not fully visible. A central question in cognitive and developmental science is how we come to have these complete mental representations, or concepts, about objects. Researchers have often turned to paradigms that assess perception of object occlusion to investigate object representations. One way to identify the necessary abilities that support veridical object concepts is by studying how they develop. Occlusion perception is relatively trivial for adults, who describe relatable figures as wholes under many conditions (Kellman & Shipley, 1991
), but it represents a major challenge for young infants (Slater, Johnson, Brown, & Badenoch, 1996
). A systematic approach to studying object concept development was pioneered by Piaget (1954/1937)
, who introduced a series of tasks posed to his own children in an attempt to gain access to development of object representations, and cognition more generally, across infancy. Following Piaget, in the present article we use the term “object concept” to refer to the ability to represent objects in the absence of direct perceptual support, as when a moving object becomes hidden by an occluding surface.
For Piaget, active search, initiated by the child, was a critical feature of object concepts. Initially in postnatal development (Stages 1 and 2 of Piaget’s 6-stage theory of sensorimotor development), infants exhibited a kind of recognition memory, but this behavior was considered more passive than active. More active search behaviors emerged after 4 months, and marked the beginnings of “true” object concepts during Stage 3. These included “visual accommodation to rapid movements,” when an infant would respond to a dropped object by looking down toward the floor. This behavior became more systematic when the infant himself dropped it, and formed the basis for predictive actions based on the perceived trajectory of the object. During Stage 4, beginning at about 8 months, an infant will search actively for an object that is completely hidden, though she might reach in an incorrect location if there are multiple possible hiding sites. Search errors are gradually overcome across the second year after birth during Stages 5 and 6, as the infant becomes fully cognizant of object identity and permanence.
Perception of object occlusion has been widely investigated by researchers since Piaget. Slater et al. (1996)
used a habituation paradigm to show that newborns do not perceive unity of partly occluded objects, meaning that fragments are processed as unrelated units rather than parts of an object. By 2 months of age, infants provide evidence of unity perception under limited conditions (Johnson, 2004
; Johnson & Aslin, 1995
), and by 4 months, infants show a strong novelty preference for object parts, indicating their ability for perceptual completion (Johnson & Nanez, 1995
; Kellman & Spelke, 1983
). Subsequent studies have expanded on this work to show the importance of particular kinds of visual information, such as common motion and alignment of object parts, to successful perceptual completion in young infants (Johnson & Aslin, 1996
; Smith, Johnson, & Spelke, 2003
Other studies of object concept development have examined infants’ looking responses to events involving fully occluded objects. The reasoning is as follows: once young infants demonstrate perceptual completion they might be able to keep track of an object’s continuous existence when there is no perceptual information about it (i.e., when the object is fully occluded). Baillargeon and colleagues provided positive evidence that 5-month olds maintained a short-term representation for an object when it was out of sight, while 3.5-month olds responded inconsistently (Baillargeon, 1987
; Baillargeon, Spelke, & Wasserman, 1985
). Rosander and von Hofsten (2004)
found a dramatic improvement in oculomotor tracking of an object undergoing occlusion over the same age range, suggesting the development of a persistent representation of the moving object. Johnson, Bremner, Slater, Mason, Foster, and Cheshire (2003)
similarly found a developmental trend between 2 and 6 months in the perception of continuity of an object’s trajectory. Using oculomotor anticipation as the dependent measure, Johnson, Amso, and Slemmer (2003)
showed that 4- and 6-month olds make anticipatory eye movements to the place of an object’s reemergence following an occlusion event. Anticipatory eye movements were interpreted as an indication of the infants’ expectancy to see the object emerge from behind the occluder. Interestingly, 6-month-old infants made significantly more anticipations than 4-month olds, suggesting a more robust representation of the hidden object in the older infants. However, exposing 4-month olds to the unoccluded trajectory of the object for a short interval improved their perception in the occluded version, shifting their performance to resemble the 6-month-old infants. Thus, perception of object occlusion and continuity develops over time and is enhanced by visual experience.
Despite extensive behavioral evidence showing the developmental course of object concepts in humans, little is known about the neural mechanisms that support them. Recent studies using noninvasive techniques in human infants have started to look at neural activity correlates of object permanence. For example, Kaufman, Csibra, and Johnson (2005)
, using a 62 sensor EEG net, identified distinct oscillatory activity over right temporal cortex during an occlusion event. In an intriguing longitudinal study, Baird et al. (2002)
measured blood oxygenation using near-infrared spectroscopy and found evidence for increased activation of frontal cortex with the onset of object permanence. Although this approach is promising, these studies are quite rare and the level of analysis is necessarily coarse in scale providing evidence about which broad areas of the brain show changes in activity patterns at key ages. Research using animal models can address developmental questions quantitatively, at a finer scale, for example, the single neuron level or the level of local connectivity. Such studies are needed to help identify the important neural processes that underlie object concepts and other cognitive abilities.
Prior investigations have suggested that the ability for perception of object occlusion and object concepts is not limited to humans. For example, perception of object occlusion can occur very early in development without much visual experience in some species, as demonstrated by studies of newly hatched chicks (Regolin, Marconato, & Vallotigara, 2006
; Regolin & Vallotigara, 1995
). Classic Piagetian search paradigms have been used to explore the expression of different stages of object permanence in nonhuman primates (e.g., Ha, Kimpo, & Sackett, 1997
; Neiworth et al., 2003
; see also review in Tomasello & Call, 1997
) and other animals (see Gomez, 2005
). The data from nonhuman primates suggest that they exhibit all of the object concept stages except Stage 6 (de Blois & Novak, 1994
; Gomez, 2005
; but see Filion, Washburn, & Gulledge, 1996
). In line with the infant studies on perception of object unity described above, Sato and colleagues examined an adult chimpanzee’s (Pan troglodytes
) matching response to a broken or complete rod using partly occluded rods as samples. They showed that the chimpanzee matched the partly occluded figures to the complete rod whenever the alignment and/or movement of the two visible parts were relatable (Sato, Kanazawa, & Fujita, 1997
). Similarly, Fujita and Giersch (2005)
showed that capuchin monkeys (Cebus apella
) also perceived unity in a partly occluded rod in a matching-to-sample task as long as the sample stimulus contained relatable parts. Using an overestimation of length illusion, Fujita (2001)
tested the capacity for perceptual completion in rhesus monkeys (Macaca mulatta
). In this illusion, adult humans tend to overestimate the length of a bar that abuts the edge of a large rectangle, suggesting that they believe it continues behind the rectangle. Rhesus monkeys have a bias for a long bar as the matching-to-sample stimulus suggesting that they extend the length of the rod very much like adult humans do. In a different approach, Churchland, Chou, and Lisberger (2003)
studied the smooth pursuit eye movements of adult rhesus monkeys following targets that blinked or were physically occluded. This study showed that eye velocity was greatly reduced when targets blinked, whereas velocity was maintained during the trials in which targets were covered by a physical occluder. This pattern of results suggests that knowledge of object permanence was guiding the monkeys’ smooth pursuit when the occluder covered the targets.
These studies suggest that adult nonhuman primates perceive object unity, object persistence following occlusion, and possess classic object concepts, reinforcing their importance as an animal model for human cognition. However, differences in testing approaches make a direct comparison to human infant studies difficult. Instead of habituation or preferential looking type paradigms, in which experimenters test the spontaneous behavior of the infant, these animals were trained to respond either in matching-to-sample type tasks or to pursue a target steadily for reward, both of which require extensive learning and experience. It is not known whether untrained or unrewarded animals would spontaneously behave in a manner consistent with unity perception and perception of object occlusion. Furthermore, in these tasks, monkeys are required to make a decision, which could depend on or be influenced by more factors than the perception of the object and which could be task-specific. Finally, these data are from adult animals only and therefore do not speak to developmental processes.
The few developmental studies about object concepts in monkeys used reaching tasks analogous to those employed by Piaget (plain reach, partial-hide, full-hide, and A-not-B). Two early studies showed that the development object concepts in rhesus macaques (Wise, Wise, & Zimmermann, 1974
) and squirrel monkeys (Saimiri sciurea
) (Vaughter, Smotherman, & Ordy, 1972
) generally follow the sequence of stages described by Piaget for the human infant, although the time of acquisition differs in monkeys and humans. Visually guided reaching appears after about 2 weeks (Boothe, Kiorpes, Regal & Lee, 1982
) followed by simple searching for an object by 3–4 weeks (Wise, Wise, & Zimmermann, 1974
). Ha, Kimpo, and Sackett (1997)
showed that pigtailed macaques (Macaca nemestrina
) achieve 2-D (screen) versions of classical object concepts before 3-D (well) versions of the same tasks; success on A-not-B was achieved last. Diamond (1990)
reported that A-not-B is mastered by infant monkeys by about 4 months. Thus, the sequence of acquisition of Piagetian object concepts by infant macaques seems to follow a similar sequence to human infants, although age norms for the stages have not been established. The current state of knowledge is limited, and therefore does not permit us to fully understand the development of object concepts nor does it reveal an understanding of the underlying neural limitations on this process.
Most studies in human infants are cross-sectional. Due to the large range of individual differences often observed in behavior across infants of a given age, trends can be lost in the noise in cross-sectional studies. Longitudinal data are of great value to show developmental trends, particularly to identify critical cross-over points, but this approach is often problematic in studies of human infants. Also, sampling the range of performance along a given stimulus dimension for each individual provides information on the strength of a cognitive or perceptual ability. But to accomplish this requires demanding paradigms and multiple test sessions that are difficult to implement in young human infants. These ideals could be met using an appropriate animal model.
Because prior studies suggest that several species of nonhuman primates are capable of unity perception (Fujita, 2001
; Fujita & Giersch, 2005
; Sato et al., 1997
) and some other object concepts (Flombaum, Kundey, Santos, & Scholl, 2004
; Hood, Hauser, Anderson, & Santos, 1999
; Neiworth et al., 2003
), and the macaque monkey provides a good animal model for development of human visual functions (Boothe et al., 1982
; Boothe, Dobson, & Teller, 1985
), a nonhuman primate model would be valuable to investigate how object permanence and related concepts develop. In the present study, we examined how object concepts develop over the first 4 months of age in the pigtailed macaque monkey. We implemented an occlusion perception task using the spontaneous behavior of the monkey by tracking their eye movements while they viewed a moving ball undergoing occlusion. In order to fully benefit from comparative studies and document cognitive ability, clear parallels need to be drawn across species using similar paradigms. The task presented in this study is directly comparable to the infant human studies conducted by our group (Johnson, Amso, & Slemmer, 2003
). We were particularly interested in implementing a task with no training requirements because, as pointed out before, long training schedules can have a profound effect on results (Pascalis & Bachevalier, 1998
). Two animals were studied longitudinally to document at what age they indicate knowledge of object persistence. Our results show that very young monkeys do not consistently anticipate the ball’s reemergence following occlusion. However, this behavior changes with age, indicating that this measure of object concepts develops over time.