Interest in relations between brain and behavioral development has grown substantially in recent years. Of special interest is the development of the brain basis of social behavior. Although researchers interested in the role of experience in brain development have proposed that experience can alter brain areas involved in social development (e.g., Greenough, Black, & Wallace, 1987
), there are very little data that address this issue. Indeed, we still have little knowledge about the development of brain systems underlying the development of social behavior and cognition.
We describe age-related differences in the neural correlates of face recognition and suggest ways that these differences may be related to changes in social development that arise through the child’s interaction with the environment. We examined the neural correlates of the response to the mother’s versus a stranger’s face throughout the toddler and preschool years. We sought to better understand the development of the recognition of familiar and unfamiliar faces during a period of great developmental change in a number of cognitive and social domains.
Infants have an inherent interest in faces, which may play a pivotal role in the development of relationships with others and in the ability to recognize the emotional states and intentions of others. A substantial body of literature makes it clear that very young infants are able to discriminate familiar from unfamiliar faces. For example, behavioral measures such as looking time and habituation have shown that, from a few days of age, infants prefer to look at a familiar versus an unfamiliar face (e.g., Pascalis & de Schonen, 1994
; Pascalis, de Schonen, Morton, Derulle, & Fabre-Grenet, 1995
), imitate selected facial movements (Meltzoff & Moore, 1977
), and by 6 weeks of age, differentially imitate familiar versus unfamiliar people (Meltzoff & Moore, 1992
Evidence from electrophysiological studies shows that by about 6 months of age infants exhibit differential brain activity to familiar faces versus unfamiliar faces, and that infants’ patterns of brain activity can be influenced by how similar the unfamiliar faces are to the familiar ones (de Haan & Nelson, 1997
). Although these event-related potential (ERP) studies do not have the spatial resolution to precisely localize the source of brain electrical activity, face-specific components of the ERP as well as face-specific patterns of scalp topography suggest that the specialization of brain areas involved in face processing begins at a very early age. In adult ERP studies, an early negative component, the N170, was larger in response to faces than to other visual stimuli, peaked earlier in response to faces than to other visual stimuli, and was prominent over the right posterior scalp (e.g., Bentin, Allison, Puce, Perez, & McCarthy, 1996
). This component likely reflects perceptual aspects of encoding “facedness.” de Haan & Nelson (1999)
measured ERPs in response to familiar and unfamiliar faces (pictures of the mother’s face vs. a stranger’s face) or to familiar and unfamiliar objects (pictures of the child’s toy vs. an unfamiliar toy). In 6-month-old infants, ERP differences in responses to familiar and unfamiliar faces and objects were found as well as ERP differences to faces versus objects. An early sensory component of the ERP peaked earlier over posterior scalp locations for faces than for objects, suggesting a temporal advantage in processing faces over objects. It is possible that the early positive component observed by de Haan and Nelson is a developmental precursor of the N170, indicating that face-specific ERP components can be differentiated early in development and provide a possible neural correlate of the precocious behavioral responses to faces that have been observed.
Other components of the ERP differentiated familiar from unfamiliar stimuli in studies by de Haan & Nelson (1997
). In these studies, a middle latency negative component (the Nc) was observed. The Nc has been associated with increased attention to salient stimuli (Courchesne, 1978
; Nelson, 1994
) as well as with recognition memory (de Haan & Nelson, 1997
; Nelson, 1994
). de Haan and Nelson (1997
) observed that the Nc component was larger in response to the mother’s face than to a stranger’s face. This finding suggests that by 6 months of age, infant brain activity discriminates mother from stranger, and that infants may devote more attentional resources to processing the mother’s face. The Nc component also was larger in response to the familiar object than to an unfamiliar toy. This finding was in contrast to previous research (e.g., Nelson & Collins, 1991
), in which the response to familiar stimuli was smaller than to unfamiliar stimuli. In contrast to the de Haan and Nelson (1997
) study and the present study, the Nelson and Collins study presented infants with “briefly familiarized” rather than truly familiar stimuli. Infants were habituated to pictures, and brain responses to those pictures and new pictures were measured. Thus, at least for 6-month-olds, the Nc component may be larger for familiar stimuli only when those stimuli are well known (e.g., a toy that the child has at home) and have been familiar for a period of months rather than by virtue of a brief familiarization period during laboratory testing.
In addition to differentiating familiar from unfamiliar stimuli, the Nc component was also differentially lateralized depending on the category of stimuli. For face stimuli, the Nc differentiated familiar from unfamiliar stimuli over the right and midline frontal electrodes, but not over left frontal electrodes. For object stimuli, electrodes over the right, midline, and left frontal sites differentiated familiar from unfamiliar stimuli. Thus, the response to faces was right lateralized whereas the response to objects was bilateral in its distribution.
In one study of mother’s face recognition described earlier (de Haan & Nelson, 1999
), slow wave activity occurring late in the recording epoch also discriminated familiar from unfamiliar stimuli. Positive slow wave (PSW) activity over frontal scalp locations was larger for unfamiliar than for familiar stimuli. The PSW has been associated with memory processes. A larger PSW has been interpreted as evidence that the infant is in the process of encoding the stimulus, but has not yet formed a complete representation (Nelson, 1994
). Given that 6-month-olds are able to recognize their mother’s face, the increased PSW activity to the stranger may have reflected updating of the memory trace for the unfamiliar stimulus, which was presented repeatedly during the study.
There is some evidence that faces are “special,” and that the neural substrate for face recognition is established from very early in life (Farah, Rabinowitz, Quinn, & Liu, 2000
). A strong nativist version of this would predict that face processing should not substantially change with development, and there should be little developmental change in the neural mechanisms for face processing and recognition.
and Gauthier and Nelson (2001)
suggested that there is development in the form of increased expertise in face processing. Children at different ages may have differential expertise with different kinds of faces. There is evidence that early in life, infants’ preference for facelike stimuli changes. Newborn infants and 2-month-olds, but not infants between these ages, prefer facelike stimuli (Morton & Johnson, 1991
), suggesting that there are developmental changes in face processing early in life. One possible explanation for such changes is that they may relate to the development of increased expertise proposed by Gauthier and Nelson.
In the present study, we report results from a cross-sectional study of face recognition in children between 18 and 54 months of age. There are reasons to believe that the relative importance of the mother’s and stranger’s face may change over this interval for children, and that this may be reflected in different patterns of brain activity. For example, at 6 to 8 months of age, infants are developing specific attachments to their primary caregivers. At this age, infants prefer familiar caretakers and are beginning to display attachment behaviors such as stranger and separation anxiety. Thus, the increased amplitude of the Nc component in response to the mother’s face (de Haan & Nelson, 1997
) may be related to the increased salience and importance of the mother in the developing formation of the attachment relationship. Infants at the age tested by de Haan and Nelson (1997
) may be in the process of forming a long-lasting representation of their caretaker’s face, and may as a result devote increased attentional and mnemonic resources to the caretaker’s face, as evidenced by the larger Nc component of the ERP. Throughout the formation of the attachment relationship, the mother’s face likely continues to be an important stimulus. However, by 18 to 24 months of age, toddlers are more likely to approach a stranger (Bretherton, Stolberg, & Kreye, 1981
) and generally respond more positively to the presence of a stranger than younger infants (Bohlin & Hagekull, 1993
). By 4 years of age, children are engaged in forming relationships with people outside of the caretaking relationship, and are likely to devote more interest and exploratory behavior toward other people other than the primary caregiver, with whom they have a well-established relationship.
In the present study, we utilized an experimental paradigm similar to that used by de Haan & Nelson (1997
), but applied it to a sample of older children between 18 and 54 months of age. In light of the developmental achievements that have occurred by the late preschool period, we hypothesized that although toddlers’ brain activity would continue to be different for images of the mother’s and stranger’s face, the pattern of differentiation evidenced by the ERP would not necessarily be the same as that found in 6-month-olds. Specifically, because of the changing meaning of a stranger’s face and the mother’s face with development, we hypothesized that there would be age-related differences in ERPs to faces. These age-related differences were expected to reflect which stimulus (i.e., the mother’s or the stranger’s face) elicited more attention from children, as reflected in the amplitude of the ERP components. In contrast, we did not expect such age-related differences in the ERP to objects.
Furthermore, we had a number of predictions regarding the expected topography of the ERP for the present study. First, based on de Haan & Nelson’s (1997
) previous studies with younger infants, we anticipated a middle latency negative component (the Nc) that peaked over frontal central midline scalp locations that was different for the familiar versus unfamiliar stimuli. For faces, the Nc component was expected to be larger in amplitude and peak earlier at frontal and midline central electrodes, and be different for familiar versus unfamiliar faces at anterior midline and temporal electrodes over the right hemisphere. For objects, the Nc component was expected to be different for familiar versus unfamiliar objects at anterior midline electrodes, and temporal electrodes over both the right and left hemispheres.