In the idea that infants were born with face-sensitive 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 any preference for static face images see Johnson and Morton, for review. Because infants shortly beyond the newborn stage did not prefer schematic face patterns over scrambled faces, it was generally assumed that newborns could not discriminate faces from other stimuli.
Over the ensuing years, more than 20 papers on newborns responses to faces and face-like patterns have been published see Johnson, for review. All of these studies bar one found some evidence of discrimination of face-like patterns. Several types of explanation have now been advanced for newborn face preferences that have been observed in at least five different laboratories and in the vast majority of studies conducted.
Conclusions were combined from experiments showing the importance of the number of elements in the upper half of a bounded area or surface, the importance of a face-relevant pattern of phase contrast, and the importance of the basic face configuration as viewed at low spatial frequencies. Johnson, 6 , —, copyright Different versions of this account and a detailed discussion of their merits are reviewed in an article by Johnson et al.
After more than a decade of p. 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. At this point it is useful to differentiate between face- specific and face- sensitive mechanisms.
The notion of CONSPEC was never claimed to be face-specific tuned only and exclusively to faces , but merely sufficient in the natural environment of the newborn to pick out faces from other objects and stimuli face-sensitive. While the arguments advanced about non-face structural preferences accept that newborns have face-sensitive mechanisms, they argue that these biases are not adapted for that purpose, but are general biases in visual processing that, in combination, just happen to pick out faces in most natural environments.
The non-face structural preferences view has spawned much empirical research. The upshot of some of this research is that only a complex combination of different biases can explain the results see Johnson et al. For example, a most preferred stimulus for a newborn would involve an up—down asymmetrical pattern with more elements or features in the upper half, but only when it is within a congruently shaped bounded object or area such as an oval.
Related recent research indicates that this near optimal stimulus is improved further with the addition of the appropriate phase-contrast relations for a top-lit face see Farroni et al. Another line of research that casts doubt on non-specific structural preferences hypo-theses is evidence supporting the existence of complex face processing abilities in newborns, discussed next. These findings, usually obtained with naturalistic face images, include a preference for attractive faces Slater et al.
A fuller consideration of the details of these effects reveal that while some of them can be accounted for by the original CONSPEC notion, other experiments force the conclusion that the bias is more specific than originally hypothesized. In Figure 1. From these images it is evident that a mechanism sensitive to the arrangement of high-contrast, low-spatial frequency components of a face would be preferentially activated by i the typical configural arrangement of eye and mouth regions, ii the presence or absence of open eyes, and iii direct versus averted gaze see Farroni et al.
Thus, the notion of CONSPEC as a mechanism that biases newborns to attend to faces has, in my view, stood the test of time fairly well. More recent conceptions, however, suggest the mechanism is further tuned to detect potential communicative partners, such as faces that engage them with direct gaze Farroni et al.
Thus, the function originally attributed to CONSPEC now needs to be expanded: it is not just for detecting and orienting to any faces, but also prioritizes faces likely to seek social interaction with the infant. In this way, it may provide a developmental basis, not just for face perception, but also for social cognition in the brain in general. I should note that an important caveat to many, but not all, of the above studies is that they are conducted with newborns more than 1 day old.
While age in days is commonly reported not to have an effect on the results obtained, studies of very early learning over the first few hours of face-to-face contact need to be a priority for the future.
A neutral face with direct gaze, averted gaze, and eyes closed, as well as a fearful face, are shown. These images support the view that, at close viewing distances, information around the eyes could activate the subcortical route. When viewed from a greater distance than in a , or in the periphery, the configuration of shadowed areas that is characteristic of a naturally top- lit face could also activate the subcortical route. A large part p. In the mid s it became feasible to record high-density event-related potentials ERPs , and, principally with Michelle de Haan, we began to exploit this method to provide evidence for the specialization of cortical processing of faces see de Haan, Chapter 38, this volume.
Some of the principles we discovered have now proved useful for functional magnetic resonance imaging fMRI studies of the neurodevelopment of face processing in children see later section. Most recently, we have helped to pioneer near infrared spectroscopy NIRS as a method for studying cortical activation to faces and other social stimuli in infants and young children Blasi et al.
Thus, the investigation of CONLERN illustrates the importance of available methods in the advancement of an area of scientific inquiry. Sometimes it is better to leave a burning question until the right methods become available for addressing it. Having said this, other researchers have made significant advances in understanding the development of the cognitive p.
Although it was very controversial at the time, we made this proposal for a couple of reasons. First, evidence from other species indicated that inborn preferences for conspecifics are mediated by more primitive subcortical neural routes. This stands in contrast to early visual learning that is mediated by forebrain or cortical systems. Second, evidence on the maturation of the human visual system suggests that there is slower development of the cortical visual routes than the subcortical during postnatal development e. Johnson, Subsequently to this and related proposals e.
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Le Doux, , neuroimaging, electrophysiological, and neuropsychological studies with adults have provided evidence for a rapid, low spatial frequency, subcortical face detection system in adults that involves the superior colliculus, pulvinar, and amygdala see Johnson, for review. Evidence that the route processes low spatial frequencies comes from fMRI studies in which the pulvinar, amygdala, and superior colliculus respond to low spatial frequency information about faces, and particularly fearful faces Winston et al.
This subcortical route was insensitive to the high spatial frequency information about faces that can activate the fusiform cortex. Finally, evidence consistent with the idea that the subcortical route modulates cortical processing comes from several functional imaging studies indicating that the degree of activation of structures in the subcortical route amygdala, superior colliculus, and pulvinar predicts or correlates with the activation of cortical face processing areas George et al. However, the causal direction of this correlation remains unknown.
What is the purpose of this putative subcortical route? The proposal that follows on from the two-process model is that it serves as a developmental basis for the emerging social brain network see Johnson, This view assumes that newborns have widespread projections from the subcortical route to cortical structures, and as a consequence face detection initially activates widespread cortical activation of regions that will become incorporated into the adult social brain. Through the constraints imposed by architectural biases within different cortical regions, and through the process of interactive specialization discussed later, particular cortical regions become increasingly tuned for social stimulus processing.
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Thus, CONSPEC and the subcortical route is a critical foundation stone for each individual child to construct their cortical social brain network Johnson, Even if you grant that CONSPEC and the subcortical route are important for the ontogeny of face perception and the social brain, does this route have any relevance or importance for those who study face processing in adults?
We have investigated this question recently Tomalski et al. Contrary to most cognitive and functional imaging paradigms in adults that involve foveal presentation of faces, we presented schematic face patterns similar to those used with newborns, but as briefly flashed peripheral stimuli. We observed more rapid saccadic orienting to p. Further, consistent with a subcortical basis, this effect is only evident with temporal the visual hemifields away from the nose rather than nasal the visual hemifields next to the nose visual field input Tomalski et al.
The effect also seems be a product of fast oculomotor routes since it is not observed with manual key press responses. While we may be able to detect subtle hallmarks of the subcortical route in laboratory experimental contexts in adults, is there any substantive consequence of this processing in the real world? If this hypothesis is correct, it means that the subcortical route continues to have a vital role in social perception and cognition in adults.
As discussed earlier, research on the mechanisms underlying CONLERN was delayed for several years due to a lack of necessary methods for progressing empirical research. While the use of ERPs has informed the neurodevelopment of face processing for some time now see De Haan, Chapter 38, this volume , only in the past 5 years has fMRI been used with children on a regular basis.
Some of the hottest debates in adult cognitive neuroscience in recent years have focused on the degree to which face-sensitive markers of cortical function, such as the N ERP component, and activation of the fusiform face area FFA are selective for face processing, and how this degree of functional specificity arises in the first place see Eimer, Chapter 17, this volume. In particular, for the FFA two opposing positions have emerged in accounting for the multitude of functional imaging data from adults.
By the latter view, faces are the objects with which most adults have considerable expertise. While this debate has generated much further research with adults see Kanwisher and Barton, Chapter 7; McKone and Robbins, Chapter 9; Scott, Chapter 11, this volume , the general question of the origin of functional specialization in human cortex is primarily a developmental issue.
Specifically, the developmental question is what are the factors both intrinsic and extrinsic to the cortex that ensure that 1 we develop particular types of specialized cognitive functions relevant for our survival, such as face and language processing, and 2 these specialized functions usually end up located in approximately the same parts of cortex? While this type of explanation appears to be valid for specialized computations within subcortical structures, a variety of genetic, neurobiological, and cognitive neuroscience evidence indicates that it is, at best, only part of the story for many human cognitive functions dependent on cerebral cortex.
I have previously outlined three viewpoints on human functional brain development e. 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 face perception, this implies that p. This view fits best with the domain specificity hypothesis in the adult literature. From this perspective, it has been argued that some cortical regions become recruited for processing face stimulus information because typical humans become perceptual experts in this domain Gauthier and Nelson, This view, then, clearly fits with the expertise hypothesis in the adult literature.
A consequence of increased specialization 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 specialized for processing social stimuli and thus become recruited to face perception computations. How does the empirical evidence from the neurodevelopment of face perception fit these views? However, there are some additional effects, such as the activation of the inferior frontal and superior temporal gyrus in response to faces in 2-month-olds Tzourio-Mazoyer et al.
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 see de Haan, Chapter 38, this volume. This suggests that despite the gradual cortical specialization seen throughout the first year of life, the system continues to specialize well beyond infancy and into childhood.
More direct evidence for or against these models can be gained from fMRI developmental neuroimaging studies with children while they are engaged in face processing.
The interactive specialization view predicts that with development there will be increased selectivity fine tuning in the activation of cortical areas for specific functions such as face processing. A consequence of this more selective activation of cortical areas is that the extent of cortical tissue activated in a given task context, or in response to a particular stimulus, will decrease and become more focal as the child gets older. This contrasts with the view that such cortical functional specializations are present from birth, or that they mature in a way relatively uninfluenced by experience.
We Cohen-Kadosh and Johnson, ; Johnson et al. Encouragingly, we found some consistency across the seven developmental fMRI studies conducted to date. Collectively, these studies show that while faces activate specific areas of cortex in children, these areas may occupy more extensive or slightly different regions from those seen in adults. Further, the three most recent studies show evidence of increasing tuning of face-sensitive areas of cortex Golarai et al.
In general, these dynamic developmental changes in cortical activation were consistent with the predictions of the interactive specialization view. Future studies will no doubt focus more on the emergence of specialized face processing networks during development using functional and structural connectivity measures. To date, the study of face perception during childhood provides perhaps the richest data source for comparing theories of functional specialization in human cortex, illustrating once again the two-way interaction between face perception studies and developmental science.
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In this chapter, I have illustrated that face perception has been one of the most important domains of study for our understanding of perceptual, cognitive, and neurocognitive aspects of human development. Additionally, the domain of face perception is one of the oldest battlegrounds for resolving key issues in the nature—nurture debate going back to Darwin and then to the origins of empirical work on human infants in the s.
This viewpoint on the history of the field has, of course, reflected my personal perspective and biases. In the next two sections of the chapter I examined how developmental thinking has influenced current research and issues on adult face perception. First, evidence for a putative subcortical route for face processing in adults has been bolstered by data from newborns where evidence suggests that cortical functioning is poor.
Constructivist developmental theory is needed in developmental neuroscience
Returning to the issue raised at the beginning of this chapter, we can now reconsider the factors, both intrinsic and extrinsic to the human cortex, that ensure that we both develop specialized processing of faces, and that this specialized function usually becomes located in the same parts of cortex in adults. With regard to developing a cortex specialized for face processing, I briefly reviewed evidence that newborns preferentially look toward faces. A number of lines of evidence suggested that this newborn preference is not mediated by the same cortical structures involved in face processing in adults, and may be due to a subcortical route for face detection.
One purpose of this early tendency to fixate on faces may be to elicit bonding from adult caregivers. However, I suggest that an equally important purpose is to bias the visual input to plastic cortical circuits. This biased sampling of the visual environment over the first days and weeks of life may ensure the appropriate specialization of later developing cortical circuitry Morton and Johnson, In addition to these findings, recent work has shown that newborns prefer to look at faces that engage them in direct mutual eye gaze Farroni et al.
Usually, when we look more closely at the p.