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To appear in R. Kail (Ed.), Advances in Child Development and Behavior, Volume 36.

The Social Cognitive Neuroscience of Infancy:

Illuminating the Early Development of Social Brain Functions

Mark H Johnson1

Tobias Grossmann1

Teresa Farroni1,2

1 Centre for Brain and Cognitive Development, School of Psychology, Birkbeck, London, UK

2 University of Padua, Italy

For: Advances in Child Development and Behavior, Volume 36.

Contact Author-

Mark H Johnson

Centre for Brain and Cognitive Development

School of Psychology, Birkbeck College

The Henry Wellcome Building

Torrington Square

London WC1E 7HX

UK

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I. Introduction

II. Face Processing

A. The sensory hypothesis B. Non-face structural preferences C. Newborns have complex face representations D. Developing cortical areas for face processing

III. Eye Gaze Processing

A. Newborns detect direct gaze B. Gaze following C. Neural processing of direct gaze in infants D. Understanding eye-object relations

IV. Perception of Emotions

A. Processing emotions in the face B. Processing emotions in the voice C. Integration of emotional information from face and voice V. Interaction between Face Identity, Eye Gaze and Emotion

A. Dissociable neural pathways for face processing in adults B. Interactions between face processing pathways in adults C. Interacting face pathways in infants VI. Conclusions

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I. Introduction

A distinct network of cortical and sub-cortical structures is selectively activated when

we are presented with, or need to process, information about fellow humans. This network has

been termed the “social brain” (Brothers, 1990; Adolphs, 1999, 2003), and the specific field

of research around it has become known as “social (cognitive) neuroscience”. Although

hundreds of studies have focused on this network in adults, its origins in infancy remain

unclear. Studying the social brain in infancy is important not only for developmental

psychologists, but also for those interested in fundamental questions about the adult system.

For example, there is a long-standing debate in the adult literature about the degree to which a

cortical area known to be activated by faces, the “fusiform face area” (Kanwisher, 1997), is

specifically dedicated for processing this type of stimulus (to the exclusion of others). While

some argue that the region undertakes (face) category-specific processing (Kanwisher, 2000),

others have presented evidence that the region can be recruited by any class of stimulus to

which the participant acquires perceptual expertise (Gauthier et al., 1999). Evidence relevant

to this debate comes from developmental studies in which the effects of experience can be

more easily assessed (Cohen-Kadosh & Johnson, in press). More importantly, accounts of the

emergence of specialised functions in the brain that are inspired by developmental

considerations can reconcile apparently conflicting views based only on data from adults

(Johnson, 2005).

The earliest stage of postnatal development, infancy (0-2 years), is the time of life

during which the most rapid changes take place. The dependent newborn seems almost a

different species from the active, inquisitive 2-year-old toddler. During this period, human

infants are faced with at least two vital and daunting challenges. The first is to understand

their physical world and its properties, such as that objects still exist even when they are out

of sight, are solid, and tend to fall downwards from tables. The second major challenge is for

the infant to gain understanding of the social world, filled with other people, including

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parents, siblings, other family members. Learning how to act in the physical world is difficult,

but it is generally predictable in the sense that most events are contingent and highly

replicable. In contrast, learning about the social world means not only developing the ability

to predict the general behaviour and responses of fellow human beings, but also going beyond

the sensory input to understanding the intentions, beliefs and desires of others. Although the

social world has some predictability, some cues are less reliable than others, and events are

rarely exactly the same from one time to the next. Furthermore, relating socially to others has

not only profound effects on what infants feel, think, and do, it is also essential for healthy

development and for optimal functioning throughout life. Indeed, the ability to learn from

other humans is perhaps one of the most important adaptations of our species (Csibra &

Gergely, 2006). Therefore, developing an understanding of other people is arguably the most

fundamental task that infants face in learning about their world.

The development of the brain circuitries involved in all kinds of cognitive processes

depends upon the interaction of two broad factors: nature (our inheritance or genetic factors),

and nurture (environmental influences). If we aim to understand how these factors interact to

‘build’ the mature social brain network, it seems of particular importance to look at how the

human brain deals with social information during infancy. In this chapter we review several

aspects of the emerging social brain in infancy from the perspective of two related theoretical

perspectives. The first of these perspectives derives from Johnson’s (2005a) updated version

of Johnson and Morton’s (1991; Morton & Johnson 1991) two-process model. The original

two-process theory sought to reconcile apparently conflicting lines of evidence about the

development of face processing by postulating the existence of two systems: a tendency for

newborns to orient to faces (Conspec), and an acquired specialisation of cortical circuits for

other aspects of face processing (Conlern). We hypothesised that Conspec served to bias the

input to developing cortical circuitry over the first weeks and months of life thus ensuring that

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appropriate cortical specialisation occurred in response to the social and survival-relevant

stimulus of faces.

The Conspec notion occupies the middle ground between those who argue that face

preferences in newborns are due to low-level psychophysical biases, and others who propose

that infants’ representations of faces are, in fact, richer and more complex than we supposed

(which we describe in detail in the next section). Johnson and Morton (1991) speculated that

Conspec was mediated largely, but not necessarily exclusively, by subcortical visuo-motor

pathways. Briefly, this proposal was made for several reasons: (a) that the newborn

behavioural preference declined at the same age as other newborn reflexes assumed to be

under sub-cortical control, (b) evidence from the maturation of the visual system indicating

later development of cortical visual pathways (e.g. Johnson, 1990), and (c) evidence from

another species (the domestic chick) (see Horn, 2004).

Subsequently, cognitive neuroscience, electrophysiological and neuropsychological

studies with adults provided evidence for a rapid, low spatial frequency, sub-cortical face

detection system in adults that involves the superior colliculus, pulvinar and amygdala

(Johnson, 2005). For example, evidence from patients with hemi-spatial neglect indicates that

they display visual extinction to stimuli in the neglected field unless arranged in the pattern of

a face (Vuilleumier, 2000; Vuilleumier & Sagiv, 2001). Vuilleumier uses this and other

evidence to propose that the human amygdala is part of a low spatial frequency sub-cortical

face processing route that boosts cortical processing of faces when these stimuli are most

relevant – a system for “emotional attention.” These and other lines of evidence strongly

support the view that there is a ‘quick and dirty’ neural route for face processing in adults, and

that this same system operates in young infants, including newborns (Johnson, 2005).

The second theoretical perspective that motivates this review of the social brain in

infancy concerns a model of functional organisation in the cerebral cortex called “Interactive

Specialisation.” Johnson (2001) presented three distinct, but not necessarily mutually

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exclusive, frameworks for understanding postnatal development in humans. According to a

“Maturational” perspective, functional brain development involves the sequential coming “on

line” of a number of modular cortical regions. The maturation of a given region is thought to

allow or enable advances in the perceptual, cognitive, or motor abilities of the child. As

applied to the neurodevelopment of social cognition, this implies that more complex aspects

(such as “theory of mind” computations) will depend on the maturation of associated cortical

regions (possibly within the prefrontal cortex). The second perspective, “Skill learning,”

argues for parallels between the dynamic brain events associated with the acquisition of

complex perceptual and motor skills in adults, and the changes in brain function seen as

infants and children come to successfully perform simpler tasks. From this perspective, it has

been argued that some cortical regions become recruited for processing social information

because typical humans become perceptual experts in this domain (Gauthier & Nelson, 2001).

A third perspective, “Interactive specialisation,” posits that functional brain development, at

least in cerebral cortex, involves a process of specialisation in which regions go from initially

having very broadly tuned functions, to having increasingly finely tuned (more specialised)

functions (Johnson, 2001). A consequence of increased specialisation of cortical regions is the

increasingly focal patterns of cortical activation resulting from a given task demand or

stimulus. By this view, some regions of cortex gradually become increasingly specialised for

processing social stimuli and thus become recruited into the social brain network.

In this chapter, we use the sub-cortical route hypothesis, and the interactive

specialisation model, to review and interpret studies on the development of face perception

and indentity, eye gaze perception, and the perception of emotional expressions. We then

discuss how these different facets of social brain function interact, and speculate on useful

directions for future research.

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II. Face processing

The face provides a wealth of socially relevant information. To detect and recognise

faces is therefore commonly considered to be an important adaptation of social animals. From

birth, human infants preferentially attend to some face-like patterns (Morton & Johnson,

1991; Johnson, 2005) suggesting a powerful mechanism to bias the input that is processed by

the newborn’s brain. Perhaps the most controversial aspect of the two-process theory was the

proposal that “infants possess some information about the structural characteristics of faces

from birth” (Morton & Johnson, 1991, p. 164). Although this committed us to the view that

the general configuration that composes a face was important, we did not commit to a specific

representation. Nevertheless, our empirical observation from the early experiments with

newborns, and evidence from other species, indicated that a stimulus with three high-contrast

blobs corresponding to the approximate location of the eyes and mouth might be sufficient. A

stimulus that appeared minimally sufficient to activate this representation (Figure 1) was

termed “Config”. We did not claim that this stimulus was identical to the representation

supporting the hypothesised Conspec system, and we remained open to the view that more

ideal stimuli for activating Conspec could potentially be created. At the time of publication

the idea that infants were born with face-specific information had been rejected by most in the

field, largely on the basis of experiments with 1- and 2-month-old infants that failed to show

face preferences (see Johnson & Morton 1991 for review). Because infants beyond the

newborn stage did not prefer schematic faces over scrambled faces, it was concluded that

newborns could not discriminate faces from other stimuli.

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INSERT FIGURE 1 about here

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At present, the Conspec notion occupies the middle ground between those who argue

that face preferences in newborns are due to low-level psychophysical biases, and others who

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propose that infants’ representations of faces are, in fact, richer and more complex than we

supposed. We will defend the view that configurational information about faces is important,

and argue that this configurational information is sufficient to account for most of the

currently available evidence pertaining to schematic and naturalistic face-like images.

Between 1991 and 2007, there were at least 16 studies conducted on face preferences in

newborns (see Johnson, 2005 for review). All of these studies found some evidence of

discrimination of face-like patterns. However, one study failed to demonstrate a preference

for face configuration (Easterbrook et al., 1999). In this study the authors failed to find

evidence of preferential tracking of face-like patterns, but did find discrimination between

face and non-face-like patterns in a habituation-dishabituation procedure. In considering the

reasons for this apparent failure to replicate it is useful to refer to the reasons why Johnson et

al. (1991) changed their procedure for testing infants after the newborn period. Specifically,

they found that the procedure of moving the test stimulus around the newborn’s head, and

measuring the extent of eye and head turning to keep the stimulus in view, was not effective

after the immediate newborn period due to maximal (ceiling) tracking to all patterned stimuli.

They therefore used a different testing procedure in which the infant was oriented relative to

the stimulus. In the experiments conducted by Easterbrook and colleagues, all of the

patterned stimuli used elicited greater degrees of orienting than in prior studies. Although the

precise reasons for this greater extent of tracking in Easterbrook’s study are not known,

differential responding is unlikely when near-ceiling performance is achieved. This

methodological point aside, several types of explanation have been advanced for newborn

face preferences that have been observed in at least five independent laboratories and the vast

majority of studies conducted.

A. The Sensory Hypothesis: A number of authors have advanced the view that newborn

visual preferences, including those for face-related stimuli, can be accounted for simply in

terms of the relative visibility of the stimuli. For example, Kleiner and Banks (1987, Kleiner

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1993) originally argued that the “linear systems model” of infant visual preferences could be

used to account for newborn face preferences. Specifically, by this account newborn face

preferences could be accounted for in terms of a simple psychophysical measure, the energy

in the amplitude spectrum of the stimulus (following Fourier decomposition). Morton et al.

(1990) reviewed critical experiments on this topic, and concluded that even when amplitude is

held constant, phase information (roughly speaking, configuration) still influences preference

toward faces. In addition to these arguments, Johnson and Morton (1991) conducted spatial

frequency analyses on the range of schematic face stimuli discussed in their book. This

analysis revealed that although spatial frequency is an important predictor of newborn visual

preferences, stimuli with the phase appropriate for a face were always more preferred than

predicted by spatial frequency alone.

In a later revival of the sensory hypothesis, Acerra and colleagues (2002) constructed a

neural network model of visual cortical processing in infants. This model, based on four

properties of the infant visual system (the spatial frequencies related to an immature retina; the

tuning properties of neurons in area V1; the activity-dependent learning properties of both

feedforward and lateral connections in cortical areas; and the absence of interhemispheric

connections) successfully simulated the results of some of the experiments on newborns

preferences for schematic face stimuli. In one critical comparison, that between the upright

and inverted “Config” stimulus (see figure 1), differences in the spacing of high-contrast

elements relative to the outline frame yields slight differences in spatial frequency that can be

detected and amplified within the model. To produce the correct predictions for the

behavioural data simulated, however, depends precisely on the exact details of the stimuli

used in one experiment (Valenza et al. 1996). Specifically, Valenza et al. (1996) inverted the

internal facial features in their stimuli in a way that resulted in the inverted stimulus having

less regular spacing between the white and black areas than the upright case. The model

exploited and amplified this small difference in spatial frequency profile, and was not tested

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with the equivalent patterns from other newborn experiments (such as Johnson et al. 1991).

Furthermore, Bednar and Miikkulainen (2003) doubt that the Acerra et al. model will be able

to simulate results from experiments involving real faces, and especially the complex visual

scenes that newborns are exposed to in real life. This is because very small irrelevant

differences between stimuli (such as where the hairline falls on a face) would have amplified

effects on visual preferences.

B. Non-face structural preferences: Debates about the mechanisms underlying face

preferences in infants have often revolved around a contrast between structural and sensory

preferences. For much of this debate, structural preferences referred to information about the

configuration of features that compose a face. An alternative proposal is that infants’

preference behaviour to face and non-face stimuli can be explained by “domain-general”

structural preferences, such as those based on known adult “Gestalt” principles (see Simion et

al., 2003). Specifically, Simion and colleagues argue that “newborns’ preference for faces

may simply result from a number of non-specific attentional biases that cause the human face

to be a frequent focus of newborns’ visual attention” (p. 15, Simion et al., 2003). These

authors still believe that the purpose of these biases is to direct attention to faces in the natural

environment of the newborn, so that they are debating the nature of the representation(s) that

underlie this bias, not the existence of the mechanism itself.

The behavioural data discussed by Simion and colleagues is consistent with a preference

for up-down asymmetrical patterns with more elements or features being in the upper half of a

bounded object or area. Such preferences are sometimes said to be due to an upper visual

field bias (Simion, Valenza, Macchi Cassia, Turati, & Umiltà, 2002). However, all the

experiments to date indicate a crucial interdependency between the borders of the object/area

and the elements within it. Indeed, some existing experiments from this group suggest that

the shape of boundary needs to correspond with the number of elements enclosed within it

(Macchi, Valenza, Simion & Leo, submitted). Experiments that independently manipulate

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upper visual field elements and bounded areas, and experiments that measure eye movements

sufficiently to control upper/lower visual field presentation have not yet been done. Therefore

the attentional bias being discussed by these authors - a bounded object or area with a greater

number of elements or features in the upper half – is likely the product of one system or

representation rather than being independent non-specific biases.

Skepticism about the “top-heavy” account of newborn face preferences seems warranted

for a number of additional reasons. First, an assumption behind the “top-heavy” view is that a

series of non-specific biases is a computationally simpler and more parsimonious account of

newborn preference than Conspec. However, as discussed previously, the extent literature

suggests that the hypothesized underlying mechanism has, at a minimum, to integrate a

boundary with the inner elements/features. More likely, object segregation followed by

numerical assessment of the number of elements present will be required. In contrast,

Conspec has been simulated by computational neural network model in which a basic Config

representation arises within the artificial cortex as a result of spontaneous activity (Bednar &

Miikkulainen, 2003).

Another reason for doubting that an upper visual field bias alone is sufficient to account

for newborn preferences comes from studies of the effects of phase contrast (Farroni et al.,

2005). In these experiments newborn preferences for upright compared to inverted Config

patterns and photographic face images were assessed with both black elements on white (as in

previous studies) and the converse (see figure 2). If the newborns are seeking elements or

features then phase contrast should make either no difference, or possibly cause them to prefer

white elements on a black background (because lighter elements are typically closer to the

viewer in natural scenes). In contrast, if the purpose of the representation is to detect faces

then black elements on white should be more effective, because the eyes and mouth region are

recessed into the face, and appear in shadow under natural (top-down) lighting conditions.

Consistent with the latter view, we (Farroni et al., 2005) found the preference for an upright

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face only under conditions of black on white or when smaller dark blobs are placed inside the

light elements. Infants preferred face-like configurations only when some contrast relations

within the image resembled to the natural difference between the darker iris and the lighter

sclera of human eyes. This was also shown to be the case with photographic images.

Newborns seem to seek for face-like stimuli that provide them with gaze information as well.

Another area that casts doubt on the “top heavy” hypothesis is evidence taken to support

the existence of complex face processing abilities in newborns. This evidence is discussed

next.

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insert Figure 2 about here

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C. Newborns have complex face representations: Some empirical results have lead to

the hypothesis that newborns already have complex processing of faces (for review see Quinn

& Slater, 2003). These findings, usually obtained with naturalistic face images, include a

preference for attractive faces (Slater et al. 1998, 2000), data indicating that newborns are

sensitive to the presence of eyes in a face (Batki et al., 2000), and that they prefer to look at

faces with direct gaze that engage them in eye contact (Farroni et al., 2002). Such findings

have led some authors to conclude that “…face recognition abilities are well developed at

birth” (Quinn & Slater, 2003, p.4).

The usual interpretation of attractiveness preferences in older infants is that these stimuli

are seen as more face-like because they best match an average or prototypical face (e.g.

Langlois & Roggman, 1990). We note in passing that the newborn effect is not just due to

increased symmetry because no preference is found with inverted stimuli. However, if we

assume that Conspec is activated most strongly by the most typical spatial arrangement of

features (rather than equidistant blobs), then a preference for more average of typical

arrangements of facial features would be expected. Furthermore, inspection of realistic face

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images through the appropriate spatial frequency filters for newborns reveals that a

mechanism sensitive to the arrangement of high-contrast, low-spatial frequency components

of a face would be preferentially activated by (a) the typical configural arrangement of eye

and mouth regions, (b) the presence (or absence) of open eyes, and (c) direct versus averted

gaze (see Farroni et al., 2002). Clearly, the extent to which Conspec can explain newborn

responses to a variety of naturalistic faces requires further investigation. However, it is very

difficult to see how the “top-heavy” hypothesis can explain this body of data, suggesting that

this theory can only account for a narrow range of preference phenomena in newborns.

Whatever the exact basis of the newborn preference, most investigators agree that it is

sufficient to cause newborns to orient to faces in their early visual environment.

Besides the detection of faces, another important aspect is to recognise familiar faces.

Newborns first recognise their mother’s face on the basis of information from the outer

contour of the head, hairline, and the internal configuration of eyes, nose, and mouth

(Bushnell, Sai, & Mullin, 1989). But not until 6 weeks of life are infants able to do this

recognition solely on the face’s internal configuration (de Schonen & Mathivet, 1990). The

face preference observed in newborns is thought to be guided largely by subcortical brain

structures, but the maturation of visual cortical areas is necessary for the emergence of the

more sophisticated competencies underlying identity recognition from faces (for a discussion,

see Johnson, 2005).

D. Developing cortical areas for face processing: Investigations of brain areas involved

in face processing in infants have been limited by ethical and technical issues (de Haan &

Thomas, 2002). One exception has been a study by Tzourio-Mazoyer and colleagues, who

took advantage of the opportunity to perform positron emission tomography (PET) on infants

in an intensive care unit as part of a clinical follow-up (Tzourio-Mazoyer et al., 2002). In this

small-scale study, a group of six 2-month-olds were imaged while they watched a face or an

array of coloured diodes used as a control stimulus. A subtraction analysis revealed that faces

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activated a network of areas in 2-month-old infants’ brains similar to that described as the

core system for face processing in adults (Haxby, Hofman, & Gobbini, 2000). More

specifically, activation was reported in an area in infants’ right inferior temporal gyrus, which

is thought to be the homologue of the adult fusiform face area (FFA) (Kanwisher, 2000;

Gauthier et al., 1999). It is interesting to note that a cortical region that at the age of 2 months

is neuroanatomically immature (Huttenlocher & Dabholkar, 1997; Huttenlocher, 2002) and

has only a low level of metabolic activity (Chugani & Phelps, 1986; Chugani, Phelps, &

Mazziotta, 1987) can exhibit functional activity. Furthermore, as we will see later, activation

of an area in response to faces does not mean that the area is specifically tuned for this

function.

Face perception also activated bilateral inferior occipital and right inferior parietal areas

in infants. The former has been implicated in early perceptual analysis of facial features,

whereas the latter is thought to support spatially directed attention in adults (Haxby et al.,

2000). Interestingly, and contrary to what is known from adults, face processing in 2-month-

olds also recruited areas in the inferior frontal and superior temporal gyrus, which have been

identified as a part of the adult language network. One possible interpretation is that the

coactivation of face and future language networks has a facilitative effect on social

interactions guiding language learning by looking at the speaker’s face (Tzourio-Mazoyer et

al., 2002).

While bearing in mind the small sample size and non-optimal control stimulus, the study

by Tzourio-Mazoyer and colleagues provided important information on a structural level by

identifying the neural substrates of the infant face processing network. However, as

mentioned earlier, due to ethical and technical concerns with the use of neuroimaging

methods like PET and functional magnetic resonance imaging (fMRI) in infants, evidence

coming from these kinds of studies is rare. Therefore, most studies that have examined infant

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brain function rely on the more readily applicable recording of EEG measures, which provide

excellent temporal resolution but relatively poor spatial resolution.

We now discuss briefly the empirical evidence available on infants’ face processing

using event-related brain potentials (ERPs; for a more detailed review, see de Haan, Johnson,

& Halit, 2003). In adults, human faces elicit an N170 response, which is most prominent over

posterior temporal sites and is larger in amplitude and longer in latency to inverted than to

upright faces (Bentin et al., 1996; de Haan, Pascalis, & Johnson, 2002). This component is not

modulated by the inversion of monkey faces (de Haan et al., 2002), nor when upright objects

are compared to inverted objects (Bentin et al., 1996). This selective inversion effect for

human faces has been taken as evidence for a face-related processing mechanism generating

the N170.

On the basis of waveform morphology and some of its response properties, it has been

suggested that the infant N290 is a precursor to the adult N170. In these studies, infants’ and

adults’ ERPs were measured in response to upright and inverted human and monkey faces (de

Haan et al., 2002; Halit, de Haan, & Johnson, 2003). The infant N290 is a negative-going

deflection observed over posterior electrodes whose peak latency decreases from 350 ms at 3

months to 290 ms at 12 months of age (Halit et al., 2003). This is consistent with the latency

of many prominent ERP components reducing with increasing age during childhood. The

results of these studies indicate that at 12 months of age the amplitude of the infant N290, like

the adult N170, increases to inverted human but not inverted monkey faces when compared to

the upright faces. However, the amplitude of the N290 was not affected by stimulus inversion

at an earlier age (3 and 6 months).

By applying new source separation and localisation methods (Richards, 2004) to the

infant ERP data, Johnson et al. (2005) identified candidate cortical sources of the face

inversion effect. This analysis suggested that generators in the left and right lateral occipital

area, the right FFA, and the right superior temporal sulcus (STS) discriminated between

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upright and inverted faces in 3- and 12-month-olds. All three cortical areas have been

implicated in the core face processing system in adults (Haxby et al., 2000), and they also

generally overlap with the areas identified in the previously discussed PET study with 2-

month-olds (Tzourio-Mazoyer et al., 2002).

The development of the brain processes reflected in the N170/N290 continues well

beyond infancy (for a review, see Taylor, Batty, & Itier, 2004). Although latency of the adult

N170 is delayed by face inversion, no such effect is observed for the latency of the infant

N290 at any age (de Haan et al., 2002; Halit et al., 2003) and, in fact, this latency effect may

not appear until 8 to 11 years (Taylor et al., 2004). Another developmental change is that

although the amplitude of the adult N170 is larger to the monkey faces, infants’ N290 shows

the opposite pattern. A completely adult-like modulation of the amplitude of the N170 has not

been reported until 13 to 14 years (Taylor et al., 2004). The reason for these changes in the

N170 response profile during mid to late childhood remain unclear.

To date, face processing, besides speech perception (Kuhl, 2004; Dehaene-Lambertz,

Dehaene, & Hertz-Pannier, 2002), represents the best-studied aspect of the infant social brain.

The evidence available from PET and EEG/ERP studies suggests that most of the brain areas

and mechanisms implicated in adult face processing can be activated relatively early in

postnatal life. However, there are some additional effects, such as the activation of the inferior

frontal and superior temporal gyrus in 2-month-olds (Tzourio-Mazoyer et al., 2002), and the

STS generator of the inversion effect found in 3- and 12-month-olds (Johnson et al., 2005),

that do not directly map onto the mature face processing system. In addition to the extra

regions involved while infants perceive faces, another important observation in the infant ERP

work is that the infant face processing system possesses much broader response properties

which are not yet as finely tuned to upright human faces. This suggests that despite the

gradual cortical specialisation seen throughout the first year of life, the system continues to

specialise well beyond infancy. These changes in the degree of specialisation of processing,

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and the spatial extent of cortical activation, are in accordance with the interactive

specialisation perspective alluded to earlier (Johnson, 2001).

III. Eye gaze processing

An important social signal encoded in faces is eye gaze. The detection and monitoring

of eye gaze direction is essential for effective social learning and communication among

humans (Bloom, 2000; Csibra & Gergely, 2006). Eye gaze provides information about the

target of another person’s attention and expression and also conveys information about

communicative intentions and future behaviour (Baron-Cohen, 1995). Eye contact is

considered to be the most powerful mode of establishing a communicative link between

humans (Kampe, Frith, & Frith, 2003). From birth, human infants are sensitive to another

person’s gaze as reflected in their preference to look at faces that have their eyes open rather

than closed (Batki et al., 2000).

A. Newborns detect direct gaze: We (Farroni, Csibra, Simion, & Johnson, 2002) tested

newborn infants by presenting them with a pair of stimuli, one a face with eye gaze directed

straight at the newborns, and the other with averted gaze (see Figure 3). Fixation times were

significantly longer for the face with the direct gaze. Furthermore, the number of orientations

was greater with the straight gaze than with the averted gaze. These results demonstrate

preferential orienting to direct eye gaze from birth. The preference is probably a result of a

fast and approximate analysis of the visual input, dedicated to finding socially relevant stimuli

for further processing.

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insert Figure 3 around here

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To examine the specificity of this newborn preference, we conducted two further

experiments. Our goal was to see whether inverting faces has any effect on gaze perception in

newborns. If the preference for direct gaze is not found under conditions of inversion, then we

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may conclude that low-level aspects of the faces, such as symmetry or local spatial frequency,

are not the basis for the newborn preference for direct gaze in upright faces previously

observed. Furthermore, an absence of the effect with inversion would indicate that the factors

responsible for the preference require the eyes to be situated within the configuration of an

upright face. Newborns did not show significant looking time or orientation differences

between direct and averted gaze conditions when the faces were presented upside down.

These results rule out symmetry and local spatial frequency as possible explanations of the

newborn effect.

Two underlying mechanisms could account for the observed gaze preferences in

newborns. By one account, even newborns have sophisticated face processing abilities

sufficient to extract gaze direction when presented in the context of a face. By an alternative

account, the preferences of newborns are based on a primitive “Conspec” detector that

responds to an optimal configuration of high-contrast elements. Straight-on faces with direct

gaze better fit this simple template than do faces with averted gaze (see Farroni et al. 2002,

2003). To test these hypotheses, we conducted a second experiment that involved similar face

stimuli, but with averted head angles. We reasoned that a sophisticated face processing system

would be able to extract gaze direction even when head angle varied. In contrast, a simple

Conspec mechanism may only produce a preference for direct gaze under conditions where

the spacing between eyes and mouth is optimal. Changing head angle alters the relative

spacing of the two eyes and mouth, and thus may disrupt the preference seen with a straight

head. In this experiment newborns looked equally at the direct gaze and at the averted gaze,

and they oriented equally to both. The results of these experiments show that the strong

preference for faces with direct gaze depends on the eyes being situated within the context of

an upright straight-ahead face. This finding simultaneously rules out many low-level

explanations of the original result along with the suggestion that newborns may have

sophisticated eye gaze perception abilities. Rather, they are consistent with the view that

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newborns orient to direct gaze due to a primitive configuration detection system (such as

“Conspec”).

B. Gaze following: Eye gaze has also been shown to effectively cue human infants’

attention to spatial locations. Hood et al. (1998) showed that the perception of an adult’s

deviated gaze induces shifts of attention in the corresponding direction in 10- to 28-week-

olds. In their experiments they modified the standard Posner cueing paradigm (Posner, 1980)

using as a central cue the direction of gaze of a woman's face, thus creating a computer

generated eye gaze shift (see figure 4 and below for details). Infants’ eye movements toward a

peripheral target were faster when the location of the target was congruent with the direction

of gaze of a centrally presented face. In subsequent studies, we examined the visual properties

of the eyes that enable infants to follow the direction of the gaze (Farroni et al., 2000). We

tested 4-month- olds using a cueing paradigm adapted from Hood et al. (1998). Each trial

began with the stimulus face eyes blinking (to attract attention), then the pupils shifted to

either the right or the left (see Fig 4a). A target stimulus was then presented either in the same

position where the eyes were looking (congruent position) or in a location incongruent with

the direction of gaze. We found that infants looked faster at the location congruent with the

direction of gaze of the face.

---

insert Figure 4 about here

---

In a second experiment, we manipulated the stimulus face so that the whole face was

shifted to one side (right or left) while the pupils remained fixed (see Fig. 4b). In this case the

infants were faster to look in the direction in which the whole face was shifted, and not the

direction where the pupils were directed. Therefore, the infants actually followed the biggest

object with lateral motion (i.e., the face) and not the eyes.

20

In a third experiment, we used the same paradigm as in the first experiment, but this

time when the eyes were opened the pupils were already oriented to the left or right, and the

infants were not able to perceive the movement of the pupils. In this case the cueing effect

disappeared. Up to this point, the results suggested that the critical feature for eye gaze cue in

infants is the movement of the pupils, and not the final direction of the pupils.

To try to understand this cueing effect better, we did three further variants of the same

procedure (Farroni et al., 2002). In the first experiment in this series we examined the effect

of inverting the face on cueing. If infants are merely cued by motion, then an inverted face

should produce the same cueing as an upright one. To our surprise, cueing had no effect,

suggesting that the context of an upright face may be important. In the next experiment

infants saw a face with an averted gaze that then shifted to the centre. If infants are

responding just to the motion of elements they should be cued in the direction opposite to the

initial gaze. Again, no cueing effect was observed. These results did not support the

hypothesis that directed motion of elements is the only determining factor for the cueing

effects.

In the last experiment, a more complex gaze shift sequence allowed us to analyse the

importance of beginning with a period of mutual gaze: the eyes shifted from centre to averted,

and then back to centre. Here we observed a significant cueing effect. Taken together, these

results suggest that cueing effects are observed only following a period of mutual gaze with

an upright face. In other words, mutual gaze with an upright face may engage mechanisms of

attention such that the viewer is more likely to be cued by subsequent motion. In summary,

the critical features for eye gaze cueing in infants are (1) lateral motion, and (2) at least a brief

preceding period of eye contact with an upright face. Finally, eye gaze has also been shown to

effectively cue newborn infants’ attention to spatial locations, suggesting a rudimentary form

of gaze following (Farroni et al., 2004a).

21

C. Neural processing of direct gaze in infants: The question that arose next concerned

how the behaviourally expressed preference for mutual gaze and the capacity to follow gaze

are implemented in the infant brain. To test infants' sensitivity to gaze direction, we recorded

ERPs as 4-month-old infants viewed photographs of faces, some with direct gaze and some

with the eyes were averted randomly to the right or left (Farroni et al., 2002). ERPs have

been shown to be sensitive to small differences in transient brain activation due to processing

of visual stimuli in infants (Csibra, Davis, Spratling, & Johnson, 2000) and they provide the

most feasible neuroimaging method to study the brain development of healthy babies. We

hypothesized that an early preference for eye contact would facilitate the processing of faces

with direct gaze.

---

insert Figure 5 about here

---

In our analyses, we focused on the N290 component described earlier (the precursor to

the adult N170). As in previous studies with infants, the N290 component peaked around 240-

290 msec post-stimulus. Its amplitude was greater in response to direct gaze than to averted

gaze (see Figure 5) with the N290 amplitude being more negative over the medial than over

the lateral leads. No differences between left and right hemisphere were observed. By 4

months, the infant brain manifests enhanced processing of faces with direct gaze as indexed

by an increased amplitude of the infant N170 when compared to averted gaze (Farroni et al.,

2002). This finding is obtained even when the head is averted but direct mutual gaze is

maintained (Farroni, et al. 2004b). However, enhanced neural processing to faces with direct

gaze is only found when eyes are presented in the context of an upright face. Our results

indicated that at this age cortical processing of faces is enhanced with direct gaze under

similar conditions to those observed in adults. Overall, these results further the view that

22

relatively simple perceptual biases in the newborn are replaced by adult-like perceptual

processing of gaze within a few months of birth.

Furthermore, source separation and localization methods were used to identify the

cortical sources of the scalp-recorded ERP effects sensitive to eye gaze (Johnson et al., 2005).

Contrary to adults, who show specific activations associated with eye gaze perception in the

STS (Allison, Puce, & McCarthy, 2000), cortical generators localised in the fusiform gyrus

discriminated gaze direction best in infants. Although the amplitude of the N170 in infants is

modulated by eye gaze (Farroni et al., 2002; 2004b) and face orientation (de Haan et al.,

2002; Halit et al., 2003), the amplitude of the adult N170 is only affected by face inversion

but not by direction of gaze (Grice et al., 2005; Taylor, Itier, Allison, & Edmonds, 2001).

Taken together, the difference in the response properties of the infant N170 (N290) versus the

adult N170 suggest that face and eye gaze share common patterns of cortical activation early

in ontogeny which later partially dissociate and become more specialised, a developmental

change that is consistent with the Interactive Specialisation view introduced earlier (Johnson,

2001).

Another technique that can reveal brain activation missed by averaging methods is the

analysis of high-frequency oscillations in the gamma band (20-100 Hz). It is thought that

brain oscillations in the high frequency range reflect neural mechanisms by which activity of

small neuronal networks is synchronized, whereas very large networks are recruited during

slow oscillations (Buzsaki & Draguhn, 2004). Synchronous activity of oscillating networks is

a prominent feature of neural activity throughout the animal kingdom (Sejnowski & Paulsen,

2006), and it is viewed as the critical middle ground linking single-neuron activity to behavior

(Herrmann, Munk, & Engel, 2004; Engel, Fries, & Singer, 2001). Such oscillations are either

time-locked to eliciting stimuli (evoked gamma activity) or can be detected as induced gamma

activity consisting of oscillatory bursts whose latency jitters from trial to trial and its temporal

relationship with the stimulus onset is fairly loose. Hence, induced gamma activity is not

23

revealed by classical averaging techniques and specific methods based on time-varying

spectral analysis of single trials are required to detect it (Tallon-Baudry & Bertrand, 1999).

As a theoretical framework, which attempts to assign functional significance to early

evoked and late induced gamma-band responses, Herrmann and colleagues (2004) have put

forward a Match-Utilization-Model (MUM). According to this model, the early gamma-band

response reflects the matching of stimulus-related information with memory contents in

primary sensory cortex. Once a stimulus has been identified through this matching stage, this

information can be used in all kinds of more complex cognitive operations involving other

brain areas and the late induced gamma response might be a signature of such a utilization

process.

Gamma oscillations are also of special interest because they have been found to

correlate with the BOLD response used in fMRI as shown in invasive work with animals

(Niessing et al., 2005) and non-invasive studies combining EEG and fMRI in humans

(Foucher et al., 2003; Fiebach, Gruber, & Supp, 2005). In this work it also has been shown

that whereas fMRI BOLD correlated with gamma-band activity such a correlation was not

found for ERP measures (e.g. Foucher et al., 2003). These findings are consistent with a

biophysical model which suggests that increases in hemodynamic signals as measured by

fMRI are associated with a shift in the spectral mass from low to high frequencies as

measured with EEG (Kilner, Mattout, Henson, & Friston, 2005).

Grossmann, Johnson, Farroni, and Csibra (in press) examined gamma oscillations and

its relation to eye gaze perception in 4-month-old infants. This study analyzed previously

published EEG data sets taken from Farroni et al.’s (2002) and (2004b) ERP studies in which

infants were presented with upright images of female faces directing their gaze toward them

or to the side. We predicted a burst of gamma oscillation over prefrontal sites to direct gaze if

gamma oscillations are indeed related to detecting eye contact/communicative intent as

suggested by adult fMRI work (Kampe et al., 2003; Schilbach et al., 2006). Because the right

24

intraparietal sulcus (IPS) and right STS are sensitive to averted gaze in the adult brain

(Hofman & Haxby, 2000) we hypothesized that some activity over right temporo-parietal

regions would be associated with the perception of averted gaze. In addition, another group of

4-month-old infants were presented with the same face stimuli upside-down, which is thought

to disrupt configural face processing (Rodriguez et al., 1999; Turati, Sangrioli, Ruel, & de

Schonen, 2004) and infants’ preference for mutual gaze (Farroni et al., 2006). Thus, we

predicted that inverted faces would not induce activity in the gamma band that differs as a

function of eye gaze.

The data revealed that gamma oscillations varied as a function of gaze direction in the

context of an upright face, which extends previous ERP and source localization results

(Farroni et al., 2002, 2004b; Johnson et al., 2005). In support of our hypotheses, specific

effects with distinct spatial and temporal characteristics were observed depending upon

whether gaze was directed at or directed away from the infant. Direct gaze compared to

averted gaze evoked early (100 ms) increased gamma activity (20-40 Hz) at occipital

channels. Short-latency phase-locked oscillatory evoked gamma responses have been

described in the visual modality in response to brief static stimuli in infant and adult EEG

(Csibra et al., 2000; Tallon-Baudry & Betrand, 1999). In adults, evoked gamma activity is

significantly larger for items that match memory representations (Herrmann, Lenz, Junge,

Busch, & Maess, 2003; Herrmann, Munk, & Engel, 2004). For infants a face with direct gaze

may represent a more familiar and prototypical face (Farroni, Massaccesi, Menon, & Johnson,

2007), which is closer to what is represented in memory than a face with averted gaze, and

therefore elicits an enhanced evoked oscillatory response. This interpretation is supported by,

and might be linked to, findings showing an enhanced neural encoding (Farroni et al., 2002)

and better recognition of upright faces with direct gaze in infants (Farroni et al., 2007). The

modulation of the evoked gamma response in this study was observed much earlier (100 ms)

than the effect in the previous ERP study (290 ms, Farroni et al., 2002, 2004). This indicates

25

that gamma activity is a more sensitive measure of some aspects of very early brain processes

related to the discrimination of gaze direction.

As predicted, direct gaze also elicited a late (300 ms) induced gamma burst over right

prefrontal channels. Directing eye gaze at someone (i.e., making eye contact) serves as an

important ostensive signal in face-to-face interactions that helps establishing a communicative

link between two people. Successful communication between two people may well depend

crucially on the ability to detect the intention to communicate conveyed by signals directed at

the self such as making eye contact (Kampe et al., 2003). On a neural level, the medial

prefrontal cortex (MPFC) is consistently activated when gaze is directed at, but not when gaze

is averted away from, the self (Kampe et al., 2003; Schilbach et al., 2006). Because gamma

oscillations measured with EEG are correlated with the BOLD response used in fMRI

(Fiebach et al., 2006; Foucher et al., 2003), eye contact detection in 4-month-old infants may

well recruit very similar brain mechanisms as in adults. The gamma burst distributed over

right frontal cortex in infants might reflect less localized functional activity than in adults,

which is in accordance with current views of functional brain development (Johnson, 2001),

suggesting a more diffuse to a more focal pattern cortical activity with age.

Averted gaze also serves an important function during social communication by

directing the perceiver’s attention to certain locations or objects, and behavioral evidence

indicates that 4-month-olds are sensitive to this aspect of eye gaze (Farroni et al., 2003; Hood

et al., 1998). The right IPS and right STS have been identified as sensitive to averted gaze in

the adult human brain (Haxby, Hofman, & Gobbini, 2000; Hofman & Haxby, 1999). Activity

in the IPS may be specifically recruited when perceived eye gaze direction elicits a shift in

spatial attention, whereas STS is more generally associated with eye and mouth movements

(Haxby et al., 2000). Our finding of a late (300 ms) induced gamma burst in response to

averted gaze over right occipito-temporal-parietal regions might reflect similar but perhaps

more diffuse brain activations in infants.

26

In another study (Grossmann, Johnson, Farroni, & Csibra, unpublished), we further

examined how head orientation would influence the infants’ brain responses to eye gaze

direction cues observed in the gamma band. This study was based on a time-frequency

analysis performed on previously published EEG data (Farroni et al., 2004b). Infants were

presented with upright images of female faces orienting their head away from the infant but

either directing their gaze towards them or away from them. Corresponding with the findings

reported for straight head angle faces, direct gaze compared to averted gaze elicited early (100

ms) increased gamma activity (20-40 Hz) at occipital channels. However, contrary to the

previous findings (Grossmann et al., 2007), no induced gamma burst was observed over

prefrontal channels to direct gaze when the head was averted.

This suggests that although infants at the age of 4 months can discriminate between

direct and averted gaze in the context of averted heads as indicated by the increased evoked

occipital gamma activity to direct gaze, in this context, they do not yet recruit brain processes

associated with detecting eye contact as a communicative signal. Hence, it follows that by 4

months a frontal face is required to elicit activity in prefrontal brain structures involved in

social communication. This finding stands in contrast to fMRI work showing that adults show

specific activity in the prefrontal cortex in response to direct gaze even when the head is

averted from the perceiver (Kampe et al., 2003) and therefore suggests that development must

occur after 4 months which enables the human brain to detect mutual gaze from static face

representations regardless of head orientation. In a follow-up study (Grossmann, Johnson,

Farroni, & Csibra, 2007), we were able to show that when infants at this age are presented

with dynamic eye gaze cues directed at them in the context of an averted head a burst of

prefrontal gamma activity was observed. This suggests that biological motion cues (i.e., gaze

shifts) help infants to detect communicative signals and recruit frontal brain regions, which

play a fundamental role for the development of social perception and cognition (Anderson et

al., 1999).

27

Furthermore, as in the previous study using faces with a frontal orientation

(Grossmann et al., in press), we observed a late (300 ms) induced gamma burst over right

temporo-parietal regions (Grossman et al., 2007), but whereas when frontal faces were used

this burst was evoked by averted gaze, for oriented faces this activity occurred in response to

direct gaze. These seemingly contradictory findings need explanation. Our suggestion is that

the gamma activity observed over right temporo-parietal channels is associated with neural

computations integrating eye gaze direction information in relation to head angle. When the

results are revisited from this perspective, it appears that this gamma burst is observed when

eye direction is different/incongruent from the head direction (i.e., averted gaze in a frontal

face and direct gaze in an oriented face). This view is in accordance with adult fMRI data

showing increased activity in the right STS to averted gaze in frontal face (Hoffman &

Haxby, 1999) and to direct gaze in averted face (Pelphrey et al., 2004).

The finding that inverted faces did not elicit gamma band responses that differed

between direct and averted gaze is in line with, and adds further developmental evidence to,

the notion that face inversion disrupts face processing (Rodriguez et al., 1999; Turati et al.,

2004). This indicates that relatively early in development cortical structures involved in face

processing are already somewhat specialized to extract information about gaze direction from

upright faces. It further shows that the gamma band effects observed in response to direct and

averted gaze are not simply driven by ‘lower level’ perceptual parameters (e.g., symmetry

[direct gaze] and asymmetry [averted gaze]) because then they should have occurred in the

inverted condition as well. These gamma band findings in infants show a high degree of

correspondence in terms of timing and frequency content with previous findings in adults

(Tallon-Baudry & Bertrand, 1999). This suggests continuity throughout development, and

further underlines the functional importance of gamma band oscillations also for social

perception.

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D. Understanding eye-object relations: Another communicative function of eye gaze is

to direct attention to certain locations, events, and objects. Understanding the relations

between eye gaze and target objects is particularly important for aspects of development such

as word learning. Comprehending that another’s gaze direction refers to a specific object

allows the child to associate the object with a name or emotional expression (Baldwin &

Moses, 1996). Adults’ gaze has been found to facilitate object processing at a neural level in

infants as young as 4 months (Reid, Striano, Kaufman, & Johnson, 2004). In this ERP study,

objects that were previously cued by eye gaze elicited a diminished positive slow wave

observed between 700 and 1000 ms over right fronto-temporal channels. A diminished

positive slow wave is thought to indicate deeper memory encoding (Nelson & Collins, 1991).

This suggests that eye gaze as a social cue facilitates brain processes involved in memory

encoding that might assist infants’ learning.

In another ERP study, 9-month-old infants and adults watched a face whose gaze

shifted either towards (object-congruent) or away from (object-incongruent) the location of a

previously presented object (Senju, Johnson, & Csibra, 2006). This paradigm was based on

that used in an earlier fMRI study (Pelphrey, Singerman, Allison, & McCarthy, 2003) and

designed to reveal the neural basis of “referential” gaze perception. When the ERPs elicited

by object-incongruent gaze shifts were compared to the object-congruent gaze shifts, an

enhanced negativity around 300 ms over occipito-temporal electrodes was observed in both

infants and adults. This suggests that infants encode referential information of gaze using

similar neural mechanisms to those engaged in adults. However, only infants showed a fronto-

central negative component that was larger in amplitude for object-congruent gaze shifts.

Thus, in the less specialised infant brain, the referential information of gaze may be encoded

in broader cortical circuits than in the more specialised adult brain.

In summary, infants show specific modulations of cortical responses associated with eye

gaze perception, which differ from what is seen in adults. Nevertheless the findings reviewed

29

also suggest that they successfully discriminate between direct and averted gaze, and can

make use of gaze cues when encoding objects in memory. This indicates that, although the

cortical structures involved in the perception of gaze direction may not be fully differentiated

in infancy, they are at least partially functional. This may be critical for social communication

and learning from others (see Disucussion).

IV. Perception of emotions

Social behaviour is coupled with emotion. During social interactions, emotions are

overtly expressed by the infant, whereas displays of emotion are normally more regulated in

adults. Nevertheless, most brain structures that are important in processing emotions in adults

are also essential for social behaviour (for a review, see Adolphs, 2003). Detecting emotion in

others through their facial expressions is an important way to communicate emotions in social

interactions (Izard, 1991). Recognising facial expressions permits us to detect another

person’s emotional state and provides cues on how to respond in these social interactions.

A. Processing emotion in the face. In an ERP study in which 7-month-olds watched

happy versus fearful faces, (Nelson & de Haan, 1996), fearful faces elicited an enhanced

negative component (Nc) peaking around 500 ms. The Nc has its maximum at frontal and

central sites and has been thought of as an obligatory attentional response sensitive to

stimulus familiarity (Courchesne, Ganz, & Norcia, 1981; Snyder, Webb, & Nelson, 2002).

Dipole modeling has revealed that the cortical sources of the Nc can be localised in the

anterior cingulate and other prefrontal regions (Reynolds & Richards, 2005). This suggests

that 7-month-old infants in Nelson and de Haan’s study allocated more attentional processing

resources to the unfamiliar fearful than to the familiar happy expression as indicated by an

enhanced Nc.

Another important question is whether infants can discriminate between different

negative emotional facial expressions. De Haan and Nelson (1997) found no difference in 7-

month-olds’ ERP responses to fearful and angry faces and suggested that infants did not

30

display different brain responses to the two expressions because they perceived the signal

value of both expressions as “negative” or because they perceived both expressions as equally

unfamiliar. In a subsequent study (Kobiella, Grossmann, Reid, & Striano, in press) using

another set of facial stimuli and measuring from more electrode positions than de Haan and

Nelson (1997), infants’ N290, P400 and Nc differed between emotions (for a discussion of

how the neural processing of angry in contrast to fearful facial expressions develops during

infancy, see Grossmann, Striano, & Friederici, 2007). This suggests that infants discriminate

between emotions of negative valence, which confirms findings that infants at this age

discriminate between the angry and fearful expressions behaviorally (Serrano, Iglesias, &

Loeches, 1995). It further suggests that the infant N290--which is viewed as the

developmental precursor to the adult N170--is sensitive to emotional information, whereas the

adult N170 does not show an emotion-dependent modulation (see also, Leppänen et al.,

2007). This suggests that early in life the N170 is sensitive to other aspects of face processing

such as eye gaze (Farroni et al., 2002) and emotional expression (Kobiella et al., in press;

Lapanen et al., 2007), a notion consistent with the Interactive Specilization view of social

brain development (Johnson, 2001, 2005).

Processing of facial expressions has been studied as a function of particular

experiences such as early institutional rearing (Parker, Nelson, & the Burcharest Intervention

Core Group, 2005) and maternal personality (de Haan et al., 2004). In general, these studies

suggest that experiential factors influence the ways that infants process facial expressions. It

is important to note that the reverse may also be true—that is, neural development occurring

at the end of the first year (Diamond, 1991, 2000; Johnson, 2001, 2005) may impact infant

behaviour and subsequently infants’ experiences with others. Although the control of infants’

orienting is partly in the hands of the caregivers’ presentation of relevant information, the

infant is clearly involved in soliciting attention and information from adults (Baldwin &

Moses, 1996; Stern, 1985). With the development of the anterior attention system during the

31

first year of postnatal life, more direct control of attention passes from the caregiver to the

infant (Bush, Luu, & Posner, 2000; Posner & Rothbart, 2000), which might influence and

regulate infants’ emotional exchanges and experiences.

B. Processing emotion in the voice. Emotion produces not only characteristic changes

in facial patterning but also in respiration, phonation, and articulation, which in turn

determine the acoustic signal (Scherer, 1989). Thus speech melody, also referred to as

emotional prosody, serves as a signal for various emotions. Adult listeners across cultures can

reliably and readily recognise different emotions on the basis of vocal cues (Banse & Scherer,

1996; Scherer, Banse, & Wallbott, 2001) and do so using some of the same brain structures

used to recognise facial expressions (Adolphs, Tranel, & Damasio, 2002). How the processing

of emotional prosody develops over the course of ontogeny is only poorly understood. Unlike

the extensive behavioural work on processing facial expressions in infancy, studies on infants’

perception of vocal expressions of emotion are relatively scarce (Walker-Andrews, 1997).

In one of the few studies of infants’ processing of emotional prosody (Grossmann,

Striano, & Friederici, 2005), infants heard semantically neutral words spoken with either a

happy, angry, or neutral voice. Angry prosody elicited a negative component peaking around

450 ms over fronto-central sites in infants’ ERPs, suggesting greater allocation of attention to

the angry prosody. This is consistent with the notion of an evolutionarily driven propensity to

react more strongly to negative than to positive or neutral stimuli (Cacioppo & Berntson,

1999). A positive slow wave (700-1000 ms) was elicited by angry and happy prosody over

temporal electrode sites, whereas words with neutral prosody returned to baseline. This

indicates an enhanced processing in auditory (temporal) brain structures of the emotionally

loaded stimuli (happy and angry), which is in line with recent fMRI work on adults’

processing of emotional speech (Grandjean et al., 2005; Mitchell et al., 2003). These findings

suggest that very early in development, the human brain detects emotionally loaded words

and shows differential attentional responses depending on their emotional valence. The three

32

emotional speech categories used in the Grossmann et al. (2005) study significantly differed

in duration and fundamental frequency but did not differ with respect to their mean intensity.

Effects due to these perceptual differences, however, are likely to be limited to early

(exogenous) ERP components (earlier than 200 ms). Therefore, acoustic differences alone

cannot account for the late ERP effects observed in response to the various emotions.

C. Integration of emotional information from face and voice. The way that emotions are

perceived when communicated either by the face or the voice has been studied in each

modality separately. However, in most social interactions, emotional information is

communicated simultaneously by different modalities such as the face and voice. Thus the

question arises: how is emotional information from the face and voice integrated? To address

this question, processing of emotionally congruent and incongruent face-voice pairs has been

studied using ERP measures (Grossmann, Striano, & Friederci, 2006). In this study, infants

watched facial expressions (happy or angry) and, after a delay of 400 ms, heard a word

spoken with a prosody that was either emotionally congruent or incongruent with the facial

expression being presented. Emotionally congruent face-voice pairs elicited similar ERP

effects as recognised items in previous memory studies with infants, children, and adults in

which a picture (visually presented)-name (acoustically presented) matching paradigm was

used (Friedman, 1991; Friedman et al., 1991, 1992; Nelson, Thomas, de Haan, & Wewerka,

1998; Rugg & Coles, 1995). Thus, the ERP effects in Grossmann et al.’s (2006) study

provides electrophysiological evidence that 7-month-olds integrate emotional information

across modalities and recognise common affect in the face and voice, a finding that is in line

with previous behavioural studies (Soken & Pick, 1992; Walker, 1982; Walker-Andrews,

1986).

Because the face-voice pairs presented to the infants were novel to them, these findings

not only indicate that infants recognised common affect but, moreover, that they applied their

knowledge about emotions in face and voice to draw inferences about what might be

33

appropriate emotional face-voice pairings. Extending previous behavioural findings, the ERP

data revealed insights into the time course and characteristics of the processes underlying the

integration of emotional information from face and voice in the infant brain. Emotionally

incongruent prosody elicited a larger fronto-central negative component (400-600 ms) in

infants’ ERPs than did an emotionally congruent prosody, indicating increased allocation of

attention. Conversely, the amplitude of infants’ positive component (600-1000 ms), with a

maximum over parietal channels, was larger to emotionally congruent than to incongruent

prosody, indexing recognition of the congruity between face and voice (Grossmann et al.,

2006).

Interestingly, the body of evidence presented here shows that effects of emotion, in

contrast to the ‘early’ effects elicited by face and gaze manipulations alone, are reflected in

specific modulations of components that occur relatively ‘late’ in the infants’ ERP (> 300 ms;

in contrast, some emotional expressions can have effects at very short-latency ERP

components in adults, Eimer & Holmes, 2002). This might be related to the fact that learning

to identify an emotion requires more complex cognitive and brain operations, which integrate

various perceptual elements provided by face and (or) voice, and retrieve specific information

about the emotion stored in memory. The studies that have been conducted so far have only

looked at a limited set of emotions (happiness, fear, and anger). This work should be extended

to other basic (disgust, sadness, surprise) and complex (social) emotions in order to

understand the emotion-specificity of the effects summarized here.

V. Interactions between face identity, eye gaze, and emotion

Following from the two theoretical frameworks that have motivated our review so far,

several specific hypotheses emerge with regard to the interaction, or lack of it, between the

different aspects of social brain function reviewed above. In this section we begin by

reviewing evidence in adults of partially independent processing streams for processing

different kinds of information from the face (identity, eye gaze, emotion). Interaction

34

between these streams appears to occur in a restricted and task-dependent way. We then go

on to review evidence from infants in support of the prediction from the interactive

specialisation view that as the social brain network develops processing streams will

fractionate and become increasingly specialised and dissociable. A specific prediction is that

infants may have a common processing stream for all aspects of face processing.

A. Dissociable neural pathways for processing faces. In adults, emotion, eye gaze, and

identity are processed by partially independent neural routes, and particular structures become

specialised for these different computations. One driver for these differential patterns of

specialization may be that different, and even conflicting, invariances need to be extracted

from the same basic visual input. For example, recognizing the identity of a face requires the

invariant aspects of facial structure configuration to be extracted from the dynamic changes

associated with eye gaze shifts and emotional expressions. An example of the neural

dissociation of these pathways comes from neuropsychological studies that provide evidence

that specific brain damage can impair the perception of facial expressions without impairment

in detecting face identity (Kurucz and Feldmar, 1979) or the face inversion perception

(Bruyer et al.,1983). Furthermore, neuroimaging studies provide evidence of a spatial and

temporal dissociation between face identity and emotion perception (Munte et al., 1998;

Sergent, Ohta, MacDonald & Zuck, 1994). Finally, different facial expressions may be

processed by different neural networks that involve both cortical regions (prefrontal, frontal

and orbital frontal cortex, occipital temporal junction, cingulated cortex and sensorial motor

cortex) and subcortical structures (amygdala, insula and basal ganglia) (Damasio et al., 2000;

Gorno-Tempini et al., 2001; Kesler-West et al. 2001; Lane et al., 1997; Streit et al., 1999).

B. Interactions between face processing pathways in adults. Although there are

dissociable routes for different aspects of face processing in adults, there are also specific

interactions between these streams of processing. These interactions can be specifically

restricted to particular stages of processing, and can be specific to particular emotions,

35

directions of eye gaze, or identities.

We begin by considering the effects of gaze direction on other aspects of face

processing. George et al. (2001) investigated how gaze direction (direct or averted),

influences face processing in adults using a gender recognition task. They presented a face

with direct or averted gaze, and the face was either a frontal view or tilted at 45 degrees.

Specific regions of the fusiform gyrus yielded stronger responses to faces when these looked

directly at the participant (regardless the orientation of the head). Because the fusiform

response can be sensitive to recognition of individuals (Gauthier et al., 2000, 1999; George et

al., 1999; Sergent et al., 1994, 1992), and is stronger for attended faces (Wojciulik et al.,

1998), the authors concluded that the stronger activity found for faces with direct gaze could

be interpreted in terms of enhanced attention and deeper encoding for faces with direct gaze

(George et al. 2001).

Furthermore, it has been previously argued that direct gaze is likely involved in the

communication of increased emotional intensity, regardless of the particular emotion being

expressed (Kimble & Olszewski, 1980; Kleinke, 1986). Despite the intuitive appeal of the

long-standing notion that direct gaze may facilitate emotional expression processing, brain

and behavioural research with adults has shown that the way in which gaze direction

influences emotion perception depends on the emotion in question (Adams & Kleck, 2003,

2005; Adams et al., 2003). There are some reasons for supporting an interaction between eye

gaze and emotional expression processing. First, analysis of facial expression and gaze

direction may be partly processed by the same anatomical structures. Areas in the superior

temporal sulcus are critical in the processing of changeable features of faces, such as

expression and gaze direction (Allison et al., 2000; Hoffman & Haxby, 2000; Perrett et al.,

1992). Neuroimaging studies have also shown that the amygdala plays a central role in

processing emotional facial expressions, particularly fear expression and fearful eyes,

(Adolphs, Tranel, Damasio, & Damasio, 1995; Breiter et al., 1996; Whalen et al., 1998, 2001)

36

and monitoring gaze direction (George et al., 2001; Wicker et al., 2003). Adams et al. (2003)

also highlighted amygdala’s involvement in the combined processing of facial expression and

gaze direction. Namely, they demonstrated that the amygdala is differentially responsive to

anger and fear expressions as a function of gaze direction.

Both eye gaze and emotional expression are reported to elicit rapid and automatic spatial

orienting (Driver et al., 1999; Öhman et al., 2001). As mentioned previously, eye gaze can

trigger orienting in automatic fashion, in that individuals shift their attention to the location of

a looked-at target in a fast and efficient manner, even when eye gaze direction is

uninformative and even counterpredictive of the target location (Driver et al., 1999; Friesen

and Kingstone, 1998, 2003). As regards emotion, many behavioural observations indicate that

people more readily pay attention to emotional than neutral stimuli. These effects also arise in

a reflexive or involuntary manner. In visual search tasks where a unique target must be found

among distractors, detection times are faster when the target has some emotional values, such

as an angry or happy face among neutral faces (Eastwood et al., 2001; Fox, 2002), or a snake

or spider among flowers (Ohman et al., 2001). Furthermore, fearful faces presented

peripherally trigger orienting of attention toward their location, thus facilitating target

discrimination at this location, more efficiently so than neutral or happy faces do (Pourtois et

al., 2004).

Finally, another reason for supporting that emotional faces may promote attention to

gaze direction is that one could expect that an expressive face (e.g., happy or fearful) gazing

in a certain direction would be a more powerful attention orienting stimulus than a

comparably gazing neutral face. Such a stimulus would provide information about another

individual’s direction of attention and, in addition, about the emotional significance of the

object or person he or she is attending to. A smiling face with an averted gaze would inform

the observer that the other person is looking at something nice or funny, whereas a

comparably gazing fearful face would suggest the presence of something threatening. So,

37

logic suggests that the gaze of an emotional face should be a more effective cue to attention.

This should be particularly true for fearful faces. Because another’s fearful gaze often signals

a source of danger, learning and/or natural selection may have particularly favoured attention

to the same location. By comparison, averted gaze in happy faces may indicate sources of

reward important for interpersonal communication, but it has less immediate relevance to

personal safety or survival.

We have seen that in adults there are complex and restricted interactions between the

different streams of face processing. Interactions can either can early in processing, such as

modulation by a fearful expression, or after the independent parallel processing of identity,

gaze and expression. These interactions are selective with, for example, specific emotions

interacting with specific directions of eye gaze.

C. Interacting face pathways in infants. A specific prediction of the Interacting

Systems model is that dissociable pathways involving specialized cortical structures in adults

may start life as un-differentiated highways of common processing in infants (Johnson 2001,

2005; Johnson & Munakata, 2005). If this is the case we should expect neural and perceptual

interactions between identity, eye gaze and emotion. However, in contrast to adults, this

interaction may be general and non-specific. In Farroni et al. (2006), we examined how facial

identity and gaze direction may interact early in infancy. The question was whether direct

gaze evokes a deeper analysis of other aspects of the person’s face such as its identity.

Specifically, we predicted that infants who had previously seen a face accompanied by direct

gaze would subsequently demonstrate recognition of that face by displaying a novelty

preference for an unfamiliar face. In contrast, we predicted no preference when infants

initially see a face with averted gaze. These predictions were confirmed. In addition, post-hoc

analyses revealed that the order in which the two conditions were presented made a

difference. If the experiment began with the direct gaze condition then the averted gaze

condition also elicited evidence of subsequent individual recognition. In contrast, if the

38

experiment began with the averted gaze condition, then only the later occurring direct gaze

condition resulted in recognition. These effects were not due to differences in looking time

between the conditions during the habituation phase. These results confirm the hypothesis that

direct gaze is an important modulator of face and social information processing early in life.

We concluded that from at least 4 months of age infants show facilitation of cueing of spatial

attention, improved individual recognition, and enhancement of neural correlates of face

processing, when accompanied, or preceded by, direct gaze.

The question of how eye gaze interacts with emotional expression has also been

examined in young infants using ERP measures (Striano, Kopp, Grossmann, & Reid, 2006).

In this study, 4-month-old infants were presented with neutral, happy, and angry facial

expressions when accompanied with direct and averted gaze. Neural processing of angry faces

was enhanced in the context of direct gaze as indexed by an increased amplitude of a late

positive fronto-central ERP component, whereas there was no effect of gaze direction on the

processing of the other expressions.

This neural sensitivity to the direction of angry gaze can be explained in two different

ways. First, infants at this age who have very rarely seen angry faces (Campos et al., 2000)

might be primed to detect novel/unfamiliar emotions that are directed toward them. Second,

infants may detect the potential threat conveyed by an angry face with gaze directed at them,

which is reflected in an enhanced neural response. To find out which explanation (‘novelty’

versus ‘threat’) can account for these ERP findings, it would be necessary to examine the

processing of a facial expression that is equally unfamiliar to the infant but whose perception

is enhanced in the context of averted gaze; one such emotion is fear (Adams et al., 2003,

Adams & Kleck, 2005). Nevertheless it is important to note that by using ERP measures it

was possible to show that the neural processing of facial expression is influenced by the

direction of eye gaze.

39

In summary, converging lines of evidence suggest more generalized interactions

between different aspects of face perception (identity, eye gaze, emotion) in infants than in

adults. These generalized interactions may be indicative of less differentiated processing

streams for these functions in infants than in adults. Greater common processing of the

different computations applied to faces in early development is a prediction of the Interactive

Specialisation approach.

VI. Conclusions

In this chapter we have illustrated how adopting a developmental cognitive

neuroscience approach sheds light on how the social brain network emerges during infancy.

We believe that the combination of neuroscience, cognitive and behavioral studies has

significantly advanced our understanding in this foundational area of neuroscience. Our work,

and that of other labs, has been presented within two frameworks; the two-process model of

the development of face-processing originally presented by Johnson & Morton (1991; Morton

& Johnson 1991) and the interactive specialization model of functional brain development

(Johnson 2001, 2005b).

With regard to the two-process model we reviewed a number of studies of newborn

face-related preferences, most of which supported the view that newborns have a bias to

orient toward faces in their natural visual environment. Although the exact mechanisms that

underlie this bias remain the topic of some debate, the proposal that best accounts for the

majority of the data currently available is that there is a “quick and dirty” sub-cortical route

for face detection that is activated by a face (or eye)-like phase contrast pattern within a

bounded surface or object (Johnson, 2005a). Interestingly, some evidence suggests a broader

role for Conspec than originally envisaged because strong evidence from adults reveals that

the “quick and dirty” sub-cortical route modulates processing in cortical regions within the

social brain network. This indicates that the mechanisms that underlie the orienting toward,

40

and foveating of, faces with direct gaze in young infants also facilitate the activation of

relevant cortical regions, providing an important foundation for the emerging social brain.

Turning to the development of social perception over the early months and years of

life, we have reviewed evidence broadly consistent with predictions from the Interactive

Specialisation approach. According to this view, most parts of the social brain network can be

activated in infants, though activation may also extend to other regions not activated under

these circumstances in adults. Furthermore, the social brain regions activated may have

broader functions (be less finely tuned) than in adults. Some of the evidence consistent with

this “Interactive Specialisation” view is that, compared to adults, infants activate regions in

addition to, and surrounding, the core face processing network. Furthermore, face and eye

gaze perception have been shown to share common patterns of cortical activation early in

ontogeny, which later partially dissociate and become more specialised (Farroni et al., 2002;

2004; Grice et al., 2005; Johnson et al., 2005; Taylor et al., 2001). These findings support the

view that structures in the social brain network initially have more homogeneous response

properties, with common processing of many aspects of faces, bodies, and actions. With

experience, these structures may become more differentiated and specialised in their response

properties, finally resulting in the specialised patterns of activation typically observed in

adults.

This view has implications for atypical development in that some developmental

disorders that involve disruption to the social brain network, such as autism, may be

characterised in terms of failures or delays of the specialisation of structures on the cortical

social brain network (see Johnson et al., 2005, for further discussion). For example, Grice et

al. (2005) found ERP evidence consistent with common processing of eye gaze and other

aspects of face perception in young children with autism, at an age at which there is evidence

for different streams of processing having emerged in typically developing children.

41

We have described several neuroimaging methods that have been used to study

different aspects of social information processing in infants. The available evidence on the

neural processes related to face, gaze, emotion, biological motion, action, and joint attention

discussed revealed how the infant brain processes information about the social world.

However, many areas of infant social cognition, such as imitation, social (complex) emotions,

and ‘theory of mind’ remain unexplored (for recent behavioural studies on infant theory of

mind, see Onishi & Baillargeon, 2005; Southgate, Senju, & Csibra, in press; Surian, Caldi, &

Sperber, in press). Future research is needed to examine the neural correlates of these more

complex aspects of social cognitive development, and it is very likely that this kind of work

will reveal greater differences between adult and infant/child brain function.

Another important issue is that although the cross-talk between developmental

psychologists and social cognitive neuroscientists has begun on a theoretical level (Decety &

Sommerville, 2004; Meltzoff & Decety, 2003), there is very little infant brain research that is

more directly informed and motivated by already existing theories of infant social cognitive

development (Csibra & Gergely, 2006, Meltzoff, 2002, 2005; Tomasello et al., 2005). The

available theoretical frameworks explaining the developmental trajectories of social cognitive

capacities provide a rich source of hypotheses that are testable using the neuroimaging tools.

In this context it will be of particular importance to identify the neural processes that underlie

known social behavioural and social cognitive transitions. Thus, further progress in the

developmental cognitive neuroscience of the social brain network crucially depends upon a

closer integration of human functional brain development with theories of social cognitive

development.

42

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Figure captions

Figure 1. Examples of schematic face stimuli used in the newborn experiments.

Figure 2. Newborns’ looking time measured in response to schematic face stimuli which

differed in their contrast polarity (Figure adapted from Farroni et al., 2005).

Figure 3. Results of the Farroni et al. (2002) preferential looking study with newborns. (a)

Mean looking times spent at two stimulus types. (b) Mean number of orientations toward each

type of stimulus. (c) Filled triangles represent reference score for the direct gaze over the

averted for each individual newborn and open triangles represent average preference scores.

Figure 4. Example of the edited video image illustrating the stimulus for Experiment 1 in

Farroni et al. (2000). In this trial the stimulus target (the duck) appears on the side which is

incongruent with the direction of gaze.

Figure 5. Four-month-old infants’ ERPs recorded to faces with direct and averted gaze in

Farroni et al. (2002). An enhanced N170 component (peaking around 240 ms after stimulus

onset) was observed over occipital cortex in response to faces with direct gaze when

compared to faces with averted gaze.

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Figure 1

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Figure 2

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Figure 3

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Figure 4

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Figure 5