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The supine position of postnatal human infantsImplications for the development of cognitive intelligence

Hideko Takeshita, Masako Myowa-Yamakoshi and Satoshi HirataSchool of Human Cultures, the University of Shiga Prefecture / Graduate School of Education, Kyoto University / Great Ape Research Institute, Hayashibara Biochemical Laboratories, Inc.

In this review, we discuss the implications of placing an infant in the supine position with respect to human cognitive development and evolution. When hu-man infants are born, they are relatively large and immature in terms of postural and locomotor ability as compared with their closest relatives, the great apes. Hence, human mothers seemingly adopt a novel pattern of caring for their large and heavy infants, i.e., placing their infants in the supine position; this promotes face-to-face communication with their infants. Moreover, infants in the supine position can interact with other nearby individuals in the same manner from an early age. In addition, the infants can also explore their own body parts and/or objects with their hands since the hands are not required to support the body and are therefore, free to move. These activities are considered to be fundamen-tal to the early development of human social and nonsocial cognition, including knowledge of self, in the first six months after birth. Further, developmental continuity in the voluntary exploratory movements in the prenatal period (in utero) to the early postnatal period is also discussed.

Keywords: supine position, neonate, fetus, humans, chimpanzees

In this review, we discuss the implications of placing an infant in the supine posi-tion with respect to human cognitive development and evolution. We approach this discussion through a framework of evolutionarily generated mother-infant inter-actions, integrating species-typical life history, maternal care practices, and infant experiences that promote a sense of self and social relationships. Confronted with

Interaction Studies 10:2 (2009), 252–268. doi 10.1075/is.10.2.08takissn 1572–0373 / e-issn 1572–0381 © John Benjamins Publishing Company

© 2009. John Benjamins Publishing CompanyAll rights reserved

Supine position in human infants 253

the difficulty of rearing infants that are born large and posturally and motorically immature, human mothers have adapted to this situation by developing a new pattern of care, i.e., placing the infants in a supine position on a solid substrate, rather than constantly holding the infant. In this case, the reduced body contact is compensated for by the increased eye contact and the slower postural and locomo-tor development, by earlier social development. This has resulted in an intimate mother-infant relationship and in the infants’ perception of self and/or objects, both of which are peculiar to humans.

A large and heavy infant

The birth weight of specific primate species can be predicted based on the weight of the females of the species (e.g., Leutenegger, 1976). In chimpanzees, the pre-dicted birth weight is around 1800 g, which is in agreement with the observed weight. On the other hand, in humans, the predicted birth weight is 1990 g, while the observed standard birth weight is generally around 3000 g (Pawlowski, 1998). While the neonatal body fat percentage is 4%–5% in chimpanzees and macaques, it is 15% in human neonates (Kuzawa, 1998). At birth, humans are the largest and heaviest among extant primates; also, they are relatively large and heavy in com-parison to their maternal body size and weight.

The observed gestational duration is around 230 days in chimpanzees and 270 days in humans, neither of which is a large deviation from the regression line for the gestational periods of placental mammals (Hofman, 1983). Thus, the non-allometric, relatively large size of human neonates suggests that this peculiarity is related to growth velocity and not gestational duration. It is likely that the gesta-tional duration is prolonged as far as possible while accounting for the constraints of morphology and physical condition; in other words, human infants are as large and heavy as they can possibly be at birth.

During the prenatal period, various primates, including humans, have similar brain-to-body weight growth curves (Deacon, 1990). That is, growth trajectories for brain and body weight are coupled in the development of primates.

Human infants not only have a larger brain and body size but also weigh more than great ape infants. The behaviors of human mothers and infants during deliv-ery have evolved differently from those exhibited by nonhuman primates, includ-ing the great apes. Kiwede (2000) reported a case of delivery in chimpanzees as follows: “At 09:22, the vagina opened wide, and the infant’s head emerged first. The infant emerged fully at 09:23:20, and KY grasped it with her left hand. The mother immediately pulled the infant onto her abdomen and hugged it.” After delivery, many primate mothers take the baby directly in their hands and immediately place


254 Hideko Takeshita, Masako Myowa-Yamakoshi and Satoshi Hirata

it on their abdomen. However, the non-allometric, relatively large size of human neonates results in an interruption of the contact between the mother and the neo-nate at delivery. Hence, from birth itself, the neonate interacts with people other than its mother while in the supine position on the ground or while being cradled by them (Rosenberg and Travathan, 1995).

Supine position: Life with the mother and siblings and interactions with other individuals

Human females developed a pattern of maternal care practice that was new to the superfamily Hominoidea in which the mothers simultaneously cared for a nursing infant and other offspring before these offspring were capable of foraging indepen-dently. Here, we will briefly discuss the following unique characteristics of human life history when compared with the great apes: emergence of childhood and care by adults other than the mother. Thereafter, we will link these characteristics to the supine position in human infants.

1. Emergence of childhoodDental development provides a useful estimate of maturation in mammals; fur-ther, it correlates with life history features. In most mammals, weaning occurs around the time when the first molar erupts. For instance, in Old World monkeys such as macaques and baboons, weaning does in fact occur when the first mo-lar erupts. However, in great apes and humans, this is not the case (Bogin, 1999; Parker & McKinney, 1999).

Smith et al. (1994) found that molar tooth development in primates shows a high correlation with brain size. In addition, the eruption of the first molar and the cessation of the increase in brain weight occur almost simultaneously. When com-pared with other primates, great apes and humans develop slowly and need a long period to achieve behavioral independence from the mother. In chimpanzees, the first molar erupts at the age of three years. However, weaning is prolonged. Chim-panzee mothers continue to care intimately for their offspring until they are five years of age or older. Human infants, on the other hand, are weaned at two to three years of age before the eruption of the first molar when they are still immature. They continue to require the assistance of older individuals, including the mother, for foraging and feeding until they mature and are able to perform these tasks independently.

Developmental retardation has evolved in humans. Both the eruption of the first molar and the cessation of the increase of brain weight are delayed; this has resulted in an increase in brain weight. Bogin dubbed the period between weaning



and the eruption of the first molar as “childhood” and suggested that this period is unique to human life history (Bogin, 1999).

2. Care by adults other than the motherIt is difficult for the mother to be engaged exclusively in rearing a nursing infant whose siblings are not yet capable of independent foraging and feeding. Since it is equally necessary to pay attention to and care for the older offspring in feeding and other contexts, the mother places the infant in the supine position so as to be able to observe the infant while taking care of the older siblings. In addition, this also allows the infant to observe the activity of the mother and others, including his/her siblings and other adults. Human females have a long life span after meno-pause, during which they can help their daughters and other young women raise offspring (Hawkes et al, 1998). In primate species that deliver babies of relatively large size, or twins, adults other than the mother often care for the babies, e.g., carrying and feeding them. It has been reported that grandmothers can reduce the burden of care for the mother in macaques (Fairbanks, 1988). Similarly, others, e.g., the grandmother, an aunt, or the father, can cradle or hold the infant. Such behavior is not exhibited by great apes. Human infants thus establish relationships not only with their mother but also with the people around her from early on; human mothers continue to rear large and heavy infants and their siblings, who continue to be dependent with regard to foraging, and establish unique social and affectionate relationships with their offspring (Greenspan & Shanker, 2004).

Thus, humans have uniquely modified their life history. These modifications must have co-occurred with changes in the mothers’ behavior in rearing offspring and thus the offspring’s development of social and nonsocial cognition.

Supine position: Face-to-face interaction

Generally, in anthropoids, infants cling to their mothers shortly after birth, and the mother supports the infant’s body whenever necessary. In several prosimian species, mothers leave the neonate in a nest when foraging. In the course of devel-opment, the mother carries the infant in her mouth or leaves the infant clinging to a branch of a tree. In prosimian species that adopt the “cling-holding” style, mothers have relatively large bodies, and weaning as well as first delivery is late (Ross, 2001).

In Hominoidea, the large body size of the female is associated with the devel-opmental retardation of the neonate and the enhancement of the mother’s caring behavior. It is easier for the great ape mothers to carry or hold their neonates, i.e., to perform a caring behavior, than for the lesser ape mothers, although the great



ape neonates are less mature than those of the lesser apes due to their reduced relative size. Prolonged, intimate infant care, a pattern which developed in the hominoid lineage, is much more developed in the great apes. A variety of playful maternal interactions, such as touching the infant’s mouth with the hand, lifting the infant up high, and increased eye contact between mother and infant, emerged as a result of this slower developmental course (Bard, 1995; Goodall, 1986; Matsu-zawa, 2006, 2007; Matsuzawa, Tomonaga, & Tanaka, 2006; Plooij, 1984).

1. Trade-off among caring stylesIt is known that chimpanzees look at the faces of other chimpanzees and make eye contact, which is a prerequisite of face-to-face communication. Recent studies demonstrated that chimpanzee mother-infant pairs often look at each other, and the frequency of this behavior doubles at one to two months of age (Bard et al., 2005; Tomonaga et al., 2004).

Neonatal smiling and neonatal imitation are seen in chimpanzees as well as in humans (Mizuno et al., 2006; Myowa-Yamakoshi et al., 2004). Similar to humans, neonatal smiling and neonatal imitation also decrease at around two months of age in chimpanzee infants when they become to be able to look at another’s face and follow it, displaying social smiling (Matsuzawa, 2006; Myowa-Yamakoshi et al., 2004; Tomonaga et al., 2004). By this time, they begin to detect the visual line of the individual whom they are facing (Myowa-Yamakoshi et al., 2003). This active approach by the chimpanzee infant resembles what is known as “the two month revolution” in humans that is characterized by the emergence of a conver-sational and contemplative stance in contrast to the earlier stimulus bound stance (Rochat, 2001). Similar to the manner in which the first socially elicited smile ap-pears at around the age of two months in human infants, the chimpanzee mother and infant also begin to look at each other and smile frequently after the infant has reached the age of two months.

A study of chimpanzee mother-infant pairs by Bard et al. (2005) revealed an inverse relationship between the amount of body contact and that of eye contact. Postures in which the body does not make contact facilitate and induce face-to-face communication, including eye contact, between the mother and her infant. In humans, face-to-face communication continues for longer periods when the infant is in the supine position rather than when it is being held (Lavelli & Fogel, 2002).

The tendency to acquire a size that is larger than what is predicted by allomet-ric rules emerged in humans in combination with the augmentation of develop-mental retardation in postural and locomotor behaviors. Moreover, in humans, the steady increase in infant size eventually made it impossible for the mother to hold the infant all the time, as the great ape mothers do. In order to care for a large, posturally immature infant with restricted locomotion, human mothers adopted



another form of caring, one that differed from the “holding-clinging” pattern that is typical of great ape mothers. Human mothers placed the infant in the supine position alongside herself; this enabled face-to-face communication including vo-calization, smiling, eye contact, and touching (Folk, 2004; Greenspan & Shanker, 2004; Matsuzawa, 2006, 2007; Parker & McKinney, 1999; Takeshita, 1999).

2. Developmental retardation of postural and locomotor behaviorsSince relevant morphology varies among primates, we introduced postural reac-tions to compare the development of postural and locomotor behaviors as a uni-tary measure (Takeshita et al., 1989; Matsuzawa, 2001).

When human infants are picked up in ways that produce the perception of gravitational instability, they show characteristic postural adjustments. In general, older infants act to orient limbs toward a substrate, or in other ways to achieve a more stable position, primarily through the extension of limbs. However, younger infants maintain flexion of the limbs under these conditions. The normative pattern of changes in postural reactions with respect to age is well known (Vojta, 1976). In fact, the clinical pediatric community uses postural adjustments to instability as a means of assessing neurobehavioral integrity. Developmental delays in the appear-ance of more mature forms of reaction to the challenge of gravitational instability can help to identify infants with cerebral palsy or other pervasive neurological dis-orders that affect motor coordination. Vojta (1976) proposed a correlation between cerebral development and developmental changes in postural adjustments.

In human infants, postural reactions change concurrently with the develop-mental changes in postural and locomotor behaviors. The most mature forms of postural reactions appear at about the same time when infants achieve bipedal locomotion. Although other species of primates typically do not walk bipedally on a routine basis, their infants do share other postural, positional, and locomo-tor patterns with human infants, such as quadrupedal locomotion and sitting. We conducted longitudinal assessments of infants in 10 primate species, includ-ing humans. Despite the fact that voluntary posture and locomotion differ among primate species, we observed a common developmental process in induced pos-tural reactions. Such reactions developed in the following four stages. In Stage 1, characterized by flexion of forelimbs and hind limbs, no reaction of the limbs to support the body is induced. In Stage 2, characterized by extension of forelimbs and flexion of hind limbs, the elbow extends with the pronation of the forearms. In Stage 3, characterized by extension of both forelimbs and hind limbs, the elbow and the knee extend with the pronation of the forearms and hind limbs. In Stage 4, characterized by a hopping reaction of the hind limbs, the hopping reaction is induced to support the body that is being tilted. While it takes about two to three months for macaque infants to develop from Stage 1 to Stage 4, it takes about 10 to



Stage 1Flexion of forelimbs and hind limbs

Stage 2Extension of forelimbs and flexion of hind limbs

Stage 3Extension of forelimbs and hind limbs

Figure 1. Development of postural reactions in primate infants induced by a treatment called Collis-horizontal (Vojta, 1976): From the top, three species of macaques (rhesus monkey, crab-eating monkey, and bonnet monkey), two species of the great apes (orang-utan and chimpanzee), and a human.(photos taken by Tetsuro Matsuzawa and Hideko Takeshita)



12 months for chimpanzee and human infants to achieve the same. To summarize, there is a progression from flexion to extension of the limbs in order to support a body that is being forced into instability by a human tester (Figure 1).

The stages of postural reactions provide a core index of motor coordination that may be readily compared across species, more appropriate than voluntary posture and locomotion and much better than chronological age. Its invariant sequence means that we can compare the duration of each phase and the age of transition to a new phase. Here, we focus on the fact that Stage 1 for humans is longer than that for chimpanzees, which, in turn, is longer than that for macaques. In other words, humans are born less mature than chimpanzees, who, in turn, are born less mature than macaques, with regard to the development of postural reactions.

A discrepancy among primates emerges between the development of postural reactions, which reflect postural and positioning abilities, and the development of voluntary posture and locomotion patterns. In chimpanzees, infants are able to walk awkwardly on four limbs when Stage 2 postural reactions begin to show at around two to three months of age. They can roll their body from supine to prone positions, crawl, and stand up quadrupedally, or bipedally by leaning on their mother’s body as well. Human infants, on the other hand, are unable to roll from supine to prone positions and remain stable in the prone position until they are about four to five months old. Interestingly, social smiling emerges at about two to three months of age in both humans and chimpanzees. In other words, in humans, social smiling emerges before the infant can support and move his/her own body, whereas in chimpanzees, it emerges with the commencement of rolling over. This suggests a notable developmental acceleration in face-to-face commu-nication, which underlies social cognition in humans, as compared to the develop-ment of posture and locomotion.

Human mothers hold, sleep alongside, and engage in face-to-face communi-cation with their infants. Thus, infants respond positively to the approach of the mother, and they actively initiate and sustain interaction from early on.

Supine position: Encountering one’s own body and objects

In most primates, the tendency of infants to cling to the mothers provides them with the opportunity to explore their mother’s body while being held by her, perceiving her warmth, softness, and smell. Supine or prone positions off the mother are both unnatural and physically unnecessary for primate neonates. Vojta (1976) described reflexive crawling and reflexive rolling over in human neonates, which are induced when the infant is placed in the prone or supine position after being separated from the mother. Separation from the mother’s body and contact with the horizontal



substrates provide the infant with the opportunity to show such reflexive move-ments, which seem to be an adaptation in order to regain contact with the mother.

1. General movementsAfter they develop appropriate postural and locomotor abilities, infant non-hu-man primates reduce contact with the mother’s body. In humans, however, being born large but with immature postural and locomotor abilities provides neonates with early opportunities to have direct contact with environmental surfaces other than the mother. Unique movements, not observed when the infant is held by the mother, emerge in the supine position. When placed in the supine position, macaque neonates roll over quickly. Chimpanzee neonates, on the other hand, are unable to roll over, but can move four limbs, unlike macaques but similar to hu-mans (Figure 2). Movements of the limbs in the supine position are called general movements (Prechtl & Hopkins, 1986).

If deterministic laws govern the system, the future movements of the limbs may be predicted, based on the motion of past values that are similar to those of the present. The predictability can be adopted as an index of complexity of move-ments of the limbs (Taga et al., 1999). We found that the complexity of general movements differs across species. While there are no significant differences in the complexity of movements between the arms and legs of chimpanzees, in humans, the movements of the arms are notably more complex than those of the legs (Ta-kaya et al., 2002). Kinematic analysis of the trajectories of the hands and feet using a nonlinear prediction method revealed a U-shaped change in humans: high com-plexity with no clear coordination among limbs at the age of one month and three months and low complexity with rhythmic movements at the age of two months (Taga et al., 1999). However, this pattern was not evident in chimpanzees (Takaya et al., 2002). The U-shaped change in general movements during normal develop-ment and the lower degree of complexity of movements in brain-damaged infants support the hypothesis that the neuromuscular system of newborns has nonlinear dynamics and that freezing and freeing of degrees of freedom plays an important role in motor development (Taga et al., 1999).

From the time when the U-shaped change occurs, which is two months after birth, manipulatory movements of the hands on the body, particularly hand-to-hand coordination (hands coming together at midline and grasping each other), occur frequently in humans.

2. Duplicated double touch experiencesHand-to-hand coordination is important because it provides the infant with dou-ble touch experiences. The tactile sensation goes both ways in reference to its own body when an infant’s hand touches its face or mouth (Rochat, 2001). For example, when the infant’s hand touches its face, the hand feels the face, while the face feels



the hand. In humans, neonates can discriminate between the finger of another person and their own when it touches their face. This suggests that they have the ability to sense and specify their own body as opposed to non-self others and/or objects in the environment (Rochat, 2001).

Rochat and Hespos (1997) demonstrated that within 24 hours of birth, hu-man neonates discriminate between self-produced tactile stimulation (self-stimu-lation) and the tactile stimulation of a non-self or of external origin (allostimula-tion). They observed the rooting responses of the neonates following stimulation of either the right or left cheek by the experimenter’s finger (allostimulation) or the spontaneous movement of one of their own hands to their own face (self-stimulation). The neonates displayed a greater tendency to turn their heads and root toward the experimenter’s finger than toward their own hands.

Among double touch experiences, hand-to-mouth coordination and hand-to-hand coordination are particularly significant; this is because the mouth and hands are both sensory-motor organs for exploration, prehension, and manipu-lation. In other words, more complex sensory-motor experiences are obtained when these two organs encounter each other rather than when the hand simply touches the cheek or another body part. By experiencing complex sensory-motor interactions involving the mouth and hands, infants come to have sense of their own body, their activity and their passivity, and hence, they develop an early per-ception-based sense of self.

3. Exploration and manipulation of objectsWhen human infants are in the supine position, manipulatory movements on the infant’s own clothing or the hands of the mother can be observed. In addition, if a toy such as a rattle is placed in the infant’s hands, the infant has the opportunity to explore an object other than its own body, long before voluntary and sophisticated reaching behavior emerges, which is at the age of four to five months.

Figure 2. Chimpanzee and orangutan infants at the age of one month are unstable when they are laid down in the supine position.(photos taken by Tetsuro Matsuzawa and Hideko Takeshita)



When compared to the development of postural reactions, the manipulation of objects among primates develops in the following manner (Takeshita et al., 1989);

1. Primate infants display a common developmental trajectory for object ma-nipulation: Voluntary and sophisticated reaching behavior emerges at Stage 2 of postural reactions, and a variety of manipulations of objects with hands develops at Stage 3.

2. More complex and variable object manipulation is observed in humans than in great apes, and more in great apes than in Old World monkeys, at the same stage of development for postural reactions. Human infants manipulate ob-jects with both hands in the stable supine position at Stages 1 to 2 of postural reactions, when they cannot sit or move by themselves. In chimpanzees, object manipulation develops after adequate postural and locomotor ability is ac-quired in Stage 3. This tendency is further emphasized in macaques in Stages 3 to 4.

The exploration of one’s own body or other objects in the supine position can be observed around two to three months of age when the human infant acquires sufficient postural control to remain stable in this posture. The supine infant re-sponds to haptic, visual, and auditory approaches, and interacts with people, while developing a greater ability to maintain the posture and a greater variety of actions unique to the posture. In particular, the exchange of vocalizations and gestures between mother and infant at this early stage of development is a feature unique to humans and one of the most important prerequisites of language acquisition (Falk 2004; Greenspan & Shanker, 2004; Takeshita, 1999).

Spontaneous movements and social responsiveness in the prenatal period

Combined with the intimate caring behavior of the mother, the immaturity of postural and locomotor abilities at birth and developmental retardation give rise to a novel type of developmental potential in human infants. We suggest that the supine position is the cradle in which features unique to human intelligence, origi-nating in the prenatal period, are nurtured.

We observed human fetuses from 2004 onwards using four-dimensional (4D) ultrasonography that enabled us to investigate fetal facial expressions and move-ments of hands and fingers through moving images scanned at several frames per second. Our study revealed that anticipatory hand-to-mouth coordination emerges at mid-gestation. Fetuses display hand-to-mouth coordination in which the mouth opens just before the approaching hand makes contact with the mouth



and the hand goes into the mouth to be sucked (Myowa-Yamakoshi & Takeshita, 2006). A smooth coordination between the movements of the approaching hand and the opening and closing of the mouth can be observed. From 20 weeks of gestational age onwards, human fetuses frequently use their hands to touch their head, face, mouth, legs, or the other hand. Through these behaviors, in principle, fetuses perhaps learn the physical relationship among body parts and obtain infor-mation about the movements of each part; this enables them to establish an early sense of self.

Further, we observed chimpanzee fetuses using 4D ultrasonography (Hirata, 2008; Myowa-Yamakoshi, 2005; Takeshita, Myowa-Yamakoshi, & Hirata, 2006; Figure 3). Three fetuses were observed from 5 to 32 weeks of gestational age; they displayed movements that were similar to those of the human fetuses.

As mentioned previously, human neonates are born with a propensity to de-velop close interactions with their mothers; this compensates for their immature postural control at birth (Falk, 2004; Greenspan & Shanker, 2004; Matsuzawa, 2006, 2007; Parker & McKinney, 1999; Takeshita, 1999). We assume that facial ex-pressions such as neonatal smiling and neonatal imitation appear to draw and hold the attention of the mother, and thus, they serve to promote the early development of the basic orientation system in human neonates. Although we have not yet fully understood the precise mechanism that enables such “social” interactions between young neonates and their mother, the facial expressions of neonates that are a part of these activities emerge and continue during fetal life (Kurjak et al., 2005).

Recent studies have revealed both neonatal smiling and neonatal imitation in chimpanzees as well (Mizuno et al., 2006; Myowa-Yamakoshi et al., 2004). Chim-panzees also manifest immature postural control at birth. Although we have not obtained clear video images of oral movements, due to the low quality of the 4D ultrasonography, which, in turn, may result from the low volume of amniotic fluid in chimpanzees, facial movements corresponding to those observed in human fe-tuses are likely to be found in chimpanzee fetuses as well. Given the above, we can state that human neonatal facial expressions that contribute to the development of mother-infant bonds might have their evolutionary origin in immature birth, which is observed in both species.

Another characteristic that draws our attention is the variety of fetal limb movements in humans. Human fetuses manifest varied limb movements in the uterine environment. The finding of the ability to discriminate between self and others through double touch experiences in human neonates suggests that this ability has already been acquired in the womb. Human fetuses make manual con-tacts with various entities in the uterine environment (e.g., the umbilical cord, uterine wall, and amniotic fluid). Active exploration of and interaction with the environment begin in the womb. Repeated exploration of the environment and



one’s own body lead to the learning of the “ecological” self (Neisser, 1995) in the course of fetal development (Myowa-Yamakoshi, 2005; Takeshita, Myowa-Yama-koshi, & Hirata, 2006).

Interestingly, the relative number of limb movements observed in a chimpan-zee fetus was low. If this difference is replicable in additional studies, the differ-ence in fetal limb movements between humans and chimpanzee fetuses might be related to the different courses of postnatal development, particularly the develop-ment of self-perception, which is more complex in human cognitive development. This study, however, raised an important issue for developmental comparisons between species: both fetal somatic and environmental constraints probably influ-ence the extent of body movements. The relative size of the fetal forelimbs to the upper body is considerably greater in chimpanzees than in humans. In contrast,

(b)

(a) (c)

Figure 3. (a) A chimpanzee mother, Tsubaki, who participated in the study that used 4D ultrasonography; (b) a chimpanzee fetus observed at 23 weeks of gestational age; and (c) a chimpanzee fetus observed at 25 weeks of gestational age.(photos taken by Satoshi Hirata, Masako Myowa-Yamakoshi, and Hideko Takeshita)



the relative size of the womb in which to move appears smaller in chimpanzees. The 2D images obtained from the 4D ultrasonography suggest that chimpanzees might have less amniotic fluid than humans. A high volume of amniotic fluid may function to facilitate the emergence of fetal motor behaviors.

Recently, Itakura et al. (2002) observed the same responses in a chimpanzee neonate as observed in humans by using the double-touch stimulus paradigm (Rochat, 2001; Rochat and Hespos, 1997). However, considerably more precise and detailed data on fetal motor behaviors in both species is needed in order to construct a coherent picture that integrates all the likely principal factors discussed above in early behavioral development. We believe that further comparative stud-ies on sensory-motor development in relation to the development of postural and locomotor ability will elucidate the evolutionary and developmental origin of co-ordinated motor behavior, advanced social cognition and the complex composi-tion of self-awareness in humans.

Acknowledgments

The authors were supported by grants from the Japan Society of the Promotion of Science (#16203034 and #20330154 to Hideko Takeshita, 16683003 and 19680013 to M. Myowa-Yama-koshi, #18700266 and #20680015 to Satoshi Hirata) during the preparation of the manuscript. The authors would like to thank Tetsuro Matsuzawa, Gen’ichi Idani, and other colleagues of the Primate Research Institute of Kyoto University, Great Ape Research Institute of Hayashibara and the “Umikaze” Infant Laboratory of the University of Shiga Prefecture for their invaluable ad-vice and support during the research. Further, the authors are grateful to Dorothy Fragaszy and James Anderson for their kind and helpful comments with respect to the earlier manuscript.

Figure 4. Changes in finger movements during hand-hand coordination made by a hu-man fetus at 25 weeks of gestational age.(photos taken by Hideko Takeshita and Masako Myowa-Yamakoshi)



References

Bard, K. A. (1995). Parenting in primates. In M. Bornstein (Ed.) Handbook of Parenting: Vol II Ecology and biology of parenting (pp. 27–58). Mahwah, NJ: Lawrence Erlbaum.

Bard, K. A., Myowa-Yamakoshi, M., Tomonaga, M., Tanaka, M., Costall, A., & Matsuzawa, T. (2005). Group differences in the mutual gaze of chimpanzees (Pan troglodytes). Develop-mental Psychology. 41, 616–624.

Bogin, B. (1999). Patterns of human growth (2nd ed.). Cambridge, UK: Cambridge University Press.

Deacon, T. (1990). Problems of ontogeny and phylogeny in brain-size evolution. International Journal of Primatology. 11, 193–236.

Fairbanks, L. A. (1988). Vervet monkey grandmothers: Effects on mother-infant relationships. Behavior. 104, 176–188.

Falk, D. (2004). Prelinguistic evolution in early hominins: Whence motherese? Behavioral and Barin Sciences. 27, 491–541.

Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Boston: Houghton Mifflin Publishing.

Greenspan, S. I., & Shanker, S. G. (2004). The first idea: How symbols, language, and intelligence evolved from our primate ancestors to modern humans. Cambridge: Da Capo Press.

Hawkes, K., O’Connell, J. F., Blurton Jones, N.G., Alvarez, H., & Charnov, E. L. (1998). Grand-mothering, menopause, and the evolution of human life histories. Proceedings of the Na-tional Academy of Science. 95, 1336–1339.

Hirata, S. (2008). Development of chimpanzee fetuses: Comparative developmental psychology for primates, 94. Hattatsu. 116, 104–112. (in Japanese)

Hofman, M. A. (1983). Evolution of brain size in neonatal and adult placental mammals: A theoretical approach. Journal of Theoretical Biology. 105, 317–332.

Itakura, S., Izumi, A., Myowa, M., Tomonaga, M., Tanaka, M., & Matsuzawa, T. (2002). Sense of self in baby chimpanzees. Conference Poster of 2nd International Workshop of Epigenetic Robotics (Edinburgh).

Kiwede, Z. T. (2000). A live birth by a primiparous female chimpanzee at the Budongo Forest. Pan Africa News. 7, 23–25.

Kurjak, A., Stanojevic, M., Andonotopo, W., Scazzocchio-Duenas, E., Azumendi, G., & Carrera, J. M. (2005). Fetal behavior assessed in all three trimesters of normal pregnancy by four-dimensional ultrasonography. Croatian Medical Journal. 46, 772–780.

Kuzawa, C. W. (1998). Adipose tissue in human infancy and childhood: An evolutionary per-spective. Yearbook of Physical Anthropology. 41, 177–209.

Lavelli, M., & Fogel, A. (2002). Developmental change in mother-infant face-to-face communi-cation: Birth to 3 months. Developmental Psychology. 38, 288–305.

Leutenegger, W. (1976). Allometory of neonatal size in eutherian mammals. Nature. 263, 229–230.

Matsuzawa, T. (2001). Primate foundations of human intelligence: A view of tool use in nonhu-man primates and fossil hominids. In T. Matsuzawa (Ed.), Primate origins of human cogni-tion and behavior (pp 3–25). Tokyo: Springer.

Matsuzawa, T. (2006). Evolutionary origins of the human-mother relationship. In T. Matsuzawa, M. Tomonaga, & M. Tanaka. (Eds.), Cognitive development in chimpanzees (pp 127–141). Tokyo: Springer.



Matsuzawa, T. (2007). Comparative cognitive development. Developmental Science. 10, 97–103.Matsuzawa, M., Tomonaga, M., & Tanaka, M. (2006). Cognitive development in chimpanzees.

Tokyo: Springer.Mizuno, Y., Takeshita, H., & Matsuzawa, T. (2006). Behavior of infant chimpanzees during the

night in the first four months of life: Neonatal smiling and sucking in relation to arousal levels. Infancy. 9, 215–234.

Myowa-Yamakoshi, M. (2005) Body and mind which emerge in the womb: Comparative devel-opmental psychology for primates, 81. Hattatsu. 103, 104–112. (in Japanese)

Myowa-Yamakoshi, M., & Takeshita, H. (2006). Do human fetuses anticipate self-oriented ac-tions? A study by four-dimensional (4D) ultrasonography. Infancy. 10, 289–301.

Myowa-Yamakoshi, M., Tomonaga, M., Tanaka, M. & Matsuzawa, T. (2003). Preference for hu-man direct gaze in infant chimpanzees (Pan troglodytes). Cognition. 89, 113–124.

Myowa-Yamakoshi, M., Tomonaga, M., Tanaka, M., & Matsuzawa, T. (2004). Imitation in neo-natal chimpanzees (Pan troglodytes). Developmental Science. 7, 437–442.

Neisser, U. (1995). Criteria for an ecological self. In P. Rochat (Ed.), The self in infancy: Theory and research. Advances in psychology 112 (pp 17–34). Amsterdam: Elsevier Science.

Parker, S. T., & McKinney, M. L. (1999). Origins of intelligence: The evolution of cognitive develop-ment in monkeys, apes, and humans. Baltimore: Johns Hopkins University Press.

Pawlowski, B. (1998). Why are human newborns so big and fat? Human Evolution. 13, 65–72.Plooij, F. X. (1984). The behavioral development of free-living chimpanzee babies and infants.

Norwood: Ablex Publishing.Prechtl, H. F. R., & Hopkins, B. (1986). Developmental transformations of spontaneous move-

ments in early infancy. Early Human Development. 4, 233–238.Rochat, P. (2001). The infant world. Cambridge: Harvard University Press.Rochat, P., & Hespos, S. J. (1997). Differential rooting response by neonates: Evidence for an

early sense of self. Early Development and Parenting. 6, 105–112.Rosenberg, K., & Travathan, W. (1995). Bipedalism and human birth: The obstetrical dilemma

revisited. Evolutionary Anthropology. 4, 161–168.Ross, C. (2001). Park or ride? Evolution of infant carrying in Primates. International Journal of

Primatology. 22, 749–771.Smith, B. H., Crummet, T. L., & Brandt, K. L. (1994). Age of eruption of primate teeth: A com-

pendium for aging individuals and comparing life histories. Yearbook of Physical Anthropol-ogy. 37, 177–231.

Taga, G., Takaya, R., & Konishi, Y. (1999). Analysis of general movements of infants towards understanding of developmental principle for motor control. Proceedings of 1999 IEEE International Conference on Systems, Man & Cybernetics. V678–683.

Takaya, R., Taga, G, & Konishi, I., Takeshita, H., Mizuno, Y., Itakura, S., Tomonaga, M., & Mat-suzawa, T. (2002). Comparative study of spontaneous movement of human and chimpan-zee infants in the first few months of life. Conference Poster of 13th International Confer-ence on Infant Studies (Tront).

Taksehita, H., Myowa-Yamakoshi, M., & Hirata, S. (2006). A new comparative perspective on prenatal motor behaviors: Preliminary research with four-dimensional utltrasonography. In T. Matsuzawa, M. Tomonaga, & M. Tanaka. (Eds.), Cognitive development in chimpan-zees (pp 37–47). Tokyo: Springer.

Takeshita, H. (1999). Early development of human mind and language: Comparative studies of behavioral development in primates. Tokyo: University of Tokyo Press. (in Japanese)



Takeshita, H., Tanaka, M., & Matsuzawa, T. (1989). Development of postural reactions and ob-ject manipulation in primate infants. Primate Research. 5, 111–120. (in Japanese with Eng-lish summary)

Takeshita, H., Mizuno, Y., & Matsuzawa, T. (2002). Development of postural reaction. M. To-monaga, M. Tanaka, & T. Matsuzawa (Eds.), Cognitive and behavioral development in chim-panzees: A comparative approach (pp 292–295). Kyoto: Kyoto University Press. (in Japa-nese)

Tomonaga, M., Tanaka, M., Matsuzawa, T., Myowa-Yamakoshi, M., Kosugi, D., Mizuno, Y., Okamoto, S., Yamaguchi, M., & Bard, K. A. (2004). Development of social cognition in in-fant chimpanzees (Pan troglodytes): Face recognition, smiling, gaze, and the lack of triadic interactions. Japanese Psychological Research. 46, 227–235.

Vojta, V. (1976). Die cerebralen Bewegungsstörungen im Säuglingsalter, Frühdiagnose, und Früh-therapie. Stuttgart: Ferdinand Enke.

Author’s addresses

Hideko Takeshita, Ph. D.School of Human Cultures, The University of Shiga PrefectureHassakacho 2500, Hikone, Shiga 522-8533, Japan

[email protected]

Masako Myowa-Yamakoshi, Ph. D.Graduate School of EducationKyoto UniversityYoshida-honmachi, Sakyo, Kyoto 606-8501, Japan

[email protected]

Satoshi Hirata, Ph. D.Great Ape Research Institute Hayashibara Biochemical Laboratories, Inc.Nu 952-2, Tamano, Okayama 706-0316, Japan

[email protected]

About the authors

Hideko Takeshita is Professor at the University of Shiga Prefecture. She organizes the “Umi-kaze” Infant Laboratory of the University of Shiga Prefecture, the longitudinal developmental studies from prenatal period to childhood. Her research interest on human development origi-nated from her studies on non-human primates including chimpanzees. She holds a Ph.D. from Kyoto University.

Masako Myowa-Yamakoshi is Associate Professor at the Graduate School of Education, Kyoto University. Her research interest is to explore the development of the human mind and its evolu-tionary foundations through the relations with socio-cultural environments. She focuses on the development of social cognition in humans and great apes such as chimpanzees and orangutans, from the fetal stage to infant stage. She holds a Ph.D. from Kyoto University.

Satoshi Hirata is Chief Scientist at the Great Ape Research Institute, Hayashibara Biochemical Laboratories, Inc. His study focuses on cognition and behavior of chimpanzees in captivity, especially their social intelligence. He holds a Ph.D. from Kyoto University.

mailto:[email protected]



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