Przemyslaw Tomalski

The two-process theory of face processing: modifications based on two decades of data from infants and adults

Johnson and Morton (1991. Biology and Cognitive Development: The Case of Face Recognition. Blackwell, Oxford) used Gabriel Horns work on the filial imprinting model to inspire a two-process theory of the development of face processing in humans. In this paper we review evidence accrued over the past two decades from infants and adults, and from other primates, that informs this two-process model. While work with newborns and infants has been broadly consistent with predictions from the model, further refinements and questions have been raised. With regard to adults, we discuss more recent evidence on the extension of the model to eye contact detection, and to subcortical face processing, reviewing functional imaging and patient studies. We conclude with discussion of outstanding caveats and future directions of research in this field.

Socioeconomic Status and Functional Brain Development--Associations in Early Infancy.

Socioeconomic status (SES) impacts on both structural and functional brain development in childhood, but how early its effects can be demonstrated is unknown. In this study we measured resting baseline EEG activity in the gamma frequency range in awake 6-9-month-olds from areas of East London with high socioeconomic deprivation. Between-subject comparisons of infants from low- and high-income families revealed significantly lower frontal gamma power in infants from low-income homes. Similar power differences were found when comparing infants according to maternal occupation, with lower occupational status groups yielding lower power. Infant sleep, maternal education, length of gestation, and birth weight, as well as smoke exposure and bilingualism, did not explain these differences. Our results show that the effects of socioeconomic disparities on brain activity can already be detected in early infancy, potentially pointing to very early risk for language and attention difficulties. This is the first study to reveal region-selective differences in functional brain development associated with early infancy in low-income families.

The effects of early adversity on the adult and developing brain

Purpose of review Recent advances in neuroimaging methods have provided new ways of unravelling the complex interplay between genetic and environmental factors that influence functional brain development in the critical first years of life. This has allowed new insights into the effects that early adverse experience can exert on the brain later in life. We review recent progress in the characterization of those effects and underlying mechanisms through which adverse environment influences the neurocognitive development. Recent findings Socioeconomic background may have a profound effect on structural and functional brain development, especially in the domains of language and prefrontal executive control. These effects are mediated by several factors: diet, quality of parental care, impoverished environment, prenatal exposure to toxic substances and so on. Other circumstances such as perinatal brain injury, early sensory deprivation or limb malformation may result in atypical functional organization of the brain and lasting cognitive impairment of certain functions. Early experience of maltreatment or institutionalized care may alter the development of the social brain, contributing to negative mental health outcomes, which may be partially reversed through early intervention programmes. Summary Subsequent models of psychiatric disorder should take into account early risk factors and embrace developmental models at multiple levels of biological organization. There is a continuing need for the study of optimal environmental input during sensitive periods in brain development.

Differential habituation to repeated sounds in infants at high risk for autism.

It has been suggested that poor habituation to stimuli might explain atypical sensory behaviours in autism. We investigated habituation to repeated sounds using an oddball paradigm in 9-month-old infants with an older sibling with autism and hence at high risk for developing autism. Auditory-evoked responses to repeated sounds in control infants (at low risk of developing autism) decreased over time, demonstrating habituation, and their responses to deviant sounds were larger than responses to standard sounds, indicating discrimination. In contrast, neural responses in infants at high risk showed less habituation and a reduced sensitivity to changes in frequency. Reduced sensory habituation may be present at a younger age than the emergence of autistic behaviour in some individuals, and we propose that this could play a role in the over responsiveness to some stimuli and undersensitivity to others observed in autism.

Rapid orienting toward face-like stimuli with gaze-relevant contrast information.

Human faces under natural illumination, and human eyes in their unique morphology, include specific contrast polarity relations that face-detection mechanisms could capitalise on. Newborns have been shown to preferentially orient to simple face-like patterns only when they contain face- or gaze-relevant contrast. We investigated whether human adults show similar preferential orienting towards schematic face-like stimuli, and whether this effect depends on the contrast polarity of the stimuli. In two experiments we demonstrate that upright schematic face-like patterns elicit faster eye movements in adult humans than inverted ones, and that this occurs only if they contain face- or gaze-relevant contrast information in the whole stimulus or in the eye region only. These results suggest that primitive mechanisms underlying the orienting bias towards faces and eyes influence and modulate social cognition not just in infants but in adults as well.

Atypical audiovisual speech integration in infants at risk for autism

The language difficulties often seen in individuals with autism might stem from an inability to integrate audiovisual information, a skill important for language development. We investigated whether 9-month-old siblings of older children with autism, who are at an increased risk of developing autism, are able to integrate audiovisual speech cues. We used an eye-tracker to record where infants looked when shown a screen displaying two faces of the same model, where one face is articulating/ba/and the other/ga/, with one face congruent with the syllable sound being presented simultaneously, the other face incongruent. This method was successful in showing that infants at low risk can integrate audiovisual speech: they looked for the same amount of time at the mouths in both the fusible visual/ga/− audio/ba/and the congruent visual/ba/− audio/ba/displays, indicating that the auditory and visual streams fuse into a McGurk-type of syllabic percept in the incongruent condition. It also showed that low-risk infants could perceive a mismatch between auditory and visual cues: they looked longer at the mouth in the mismatched, non-fusible visual/ba/− audio/ga/display compared with the congruent visual/ga/− audio/ga/display, demonstrating that they perceive an uncommon, and therefore interesting, speech-like percept when looking at the incongruent mouth (repeated ANOVA: displays x fusion/mismatch conditions interaction: F(1,16) = 17.153, p = 0.001). The looking behaviour of high-risk infants did not differ according to the type of display, suggesting difficulties in matching auditory and visual information (repeated ANOVA, displays x conditions interaction: F(1,25) = 0.09, p = 0.767), in contrast to low-risk infants (repeated ANOVA: displays x conditions x low/high-risk groups interaction: F(1,41) = 4.466, p = 0.041). In some cases this reduced ability might lead to the poor communication skills characteristic of autism.

Temporal-nasal asymmetry of rapid orienting to face-like stimuli.

Recent work suggests that a subcortical visual route may mediate rapid orienting towards faces in the visual periphery. We now demonstrate that this orienting bias towards faces shows a temporal-nasal visual field asymmetry of responses, supporting the view that it is mediated by extrageniculate pathways. Upright schematic face-like pattern elicited faster behavioural responses than inverted one in the temporal but not in the nasal hemifield of each eye. This effect occurred for saccades but not for manual responses. The presence of a similar asymmetry of the orienting bias in newborns supports the role of extrageniculate pathways in face detection in both neonates and adults.

Exploring early developmental changes in face scanning patterns during the perception of audiovisual mismatch of speech cues

Young infants are capable of integrating auditory and visual information and their speech perception can be influenced by visual cues, while 5-month-olds detect mismatch between mouth articulations and speech sounds. From 6 months of age, infants gradually shift their attention away from eyes and towards the mouth in articulating faces, potentially to benefit from intersensory redundancy of audiovisual (AV) cues. Using eye tracking, we investigated whether 6- to 9-month-olds showed a similar age-related increase of looking to the mouth, while observing congruent and/or redundant versus mismatched and non-redundant speech cues. Participants distinguished between congruent and incongruent AV cues as reflected by the amount of looking to the mouth. They showed an age-related increase in attention to the mouth, but only for non-redundant, mismatched AV speech cues. Our results highlight the role of intersensory redundancy and audiovisual mismatch mechanisms in facilitating the development of speech processing in infants under 12 months of age.

Brain responses to audiovisual speech mismatch in infants are associated with individual differences in looking behaviour

Research on audiovisual speech integration has reported high levels of individual variability, especially among young infants. In the present study we tested the hypothesis that this variability results from individual differences in the maturation of audiovisual speech processing during infancy. A developmental shift in selective attention to audiovisual speech has been demonstrated between 6 and 9 months with an increase in the time spent looking to articulating mouths as compared to eyes (Lewkowicz & Hansen‐Tift. (2012) Proc. Natl Acad. Sci. USA, 109, 1431–1436; Tomalski et al. (2012) Eur. J. Dev. Psychol., 1–14). In the present study we tested whether these changes in behavioural maturational level are associated with differences in brain responses to audiovisual speech across this age range. We measured high‐density event‐related potentials (ERPs) in response to videos of audiovisually matching and mismatched syllables /ba/ and /ga/, and subsequently examined visual scanning of the same stimuli with eye‐tracking. There were no clear age‐specific changes in ERPs, but the amplitude of audiovisual mismatch response (AVMMR) to the combination of visual /ba/ and auditory /ga/ was strongly negatively associated with looking time to the mouth in the same condition. These results have significant implications for our understanding of individual differences in neural signatures of audiovisual speech processing in infants, suggesting that they are not strictly related to chronological age but instead associated with the maturation of looking behaviour, and develop at individual rates in the second half of the first year of life.

Brain responses and looking behavior during audiovisual speech integration in infants predict auditory speech comprehension in the second year of life

The use of visual cues during the processing of audiovisual (AV) speech is known to be less efficient in children and adults with language difficulties and difficulties are known to be more prevalent in children from low-income populations. In the present study, we followed an economically diverse group of thirty-seven infants longitudinally from 6–9 months to 14–16 months of age. We used eye-tracking to examine whether individual differences in visual attention during AV processing of speech in 6–9 month old infants, particularly when processing congruent and incongruent auditory and visual speech cues, might be indicative of their later language development. Twenty-two of these 6–9 month old infants also participated in an event-related potential (ERP) AV task within the same experimental session. Language development was then followed-up at the age of 14–16 months, using two measures of language development, the Preschool Language Scale and the Oxford Communicative Development Inventory. The results show that those infants who were less efficient in auditory speech processing at the age of 6–9 months had lower receptive language scores at 14–16 months. A correlational analysis revealed that the pattern of face scanning and ERP responses to audiovisually incongruent stimuli at 6–9 months were both significantly associated with language development at 14–16 months. These findings add to the understanding of individual differences in neural signatures of AV processing and associated looking behavior in infants.