The influence of maternal anxiety and depression symptoms on fNIRS brain responses to emotional faces in 5- and 7-month-old infants

Greater relative right (versus left) frontal cortical activation to emotional faces as measured with alpha power in the electroencephalogram (EEG), has been considered a promising neural marker of increased vulnerability to psychopathology and emotional disorders. We set out to explore multichannel fNIRS as a tool to investigate infants’ frontal asymmetry responses (hypothesizing greater right versus left frontal cortex activation) to emotional faces as influenced by maternal anxiety and depression symptoms during the postnatal period. We also explored activation differences in fronto-temporal regions associated with facial emotion processing. Ninety-one typically developing 5- and 7-month-old infants were shown photographs of women portraying happy, fearful and angry expressions. Hemodynamic brain responses were analyzed over two frontopolar and seven bilateral cortical regions subdivided into frontal, temporal and parietal areas, defined by age-appropriate MRI templates. Infants of mothers reporting higher negative affect had greater oxyhemoglobin (oxyHb) activation across all emotions over the left inferior frontal gyrus, a region implicated in emotional communication. Follow-up analyses indicated that associations were driven by maternal depression, but not anxiety symptoms. Overall, we found no support for greater right versus left frontal cortex activation in association with maternal negative affect. Findings point to the potential utility of fNIRS as a method for identifying altered neural substrates associated with exposure to maternal depression in infancy.     

A brief review on the use of functional near-infrared spectroscopy (fNIRS) for language imaging studies in human newborns and adults

Upon stimulation, real time maps of cortical hemodynamic responses can be obtained by non-invasive functional near-infrared spectroscopy (fNIRS) which measures changes in oxygenated and deoxygenated hemoglobin after positioning multiple sources and detectors over the human scalp. The current commercially available transportable fNIRS systems have a time resolution of 1-10 Hz, a depth sensitivity of about 1.5 cm, and a spatial resolution of about 1 cm. The goal of this brief review is to report infants, children and adults fNIRS language studies. Since 1998, 60 studies have been published on cortical activation in the brain’s classic language areas in children/adults as well as newborns using fNIRS instrumentations of different complexity. In addition, the basic principles of fNIRS including features, strengths, advantages, and limitations are summarized in terms that can be understood even by non specialists. Future prospects of fNIRS in the field of language processing imaging are highlighted.     

Functions of parahippocampal place area and retrosplenial cortex in real-world scene analysis: An fMRI study

We used functional MRI to investigate several hypotheses concerning the functions of posterior parahippocampal cortex and retrosplenial cortex, two regions that preferentially activate to images of real-world scenes compared to images of other meaningful visual stimuli such as objects and faces. We compared activation resulting from photographs of rooms, city streets, cityscapes, and landscapes against activation to a control condition of objects. Activation in posterior parahippocampal cortex, including parahippocampal place area, was greater for all scene types than objects, and greater for scenes that clearly convey information about local three-dimensional (3-D) structure (city streets and rooms) than scenes that do not (cityscapes and landscapes). Similar differences were observed in retrosplenial cortex, though activation was also greater for city streets than rooms. These results suggest that activation in both cortical areas is primarily related to analysis or representation of local 3-D space. The results are not consistent with hypotheses that these areas reflect panoramic spatial volume, an artificial versus natural category distinction, an indoor versus outdoor distinction, or the number of explicit objects depicted in a scene image.     

Effects of aging on the neural correlates of successful item and source memory encoding

To investigate the neural basis of age-related source memory (SM) deficits, young and older adults were scanned with fMRI while encoding faces, scenes, and face-scene pairs. Successful encoding activity was identified by comparing encoding activity for subsequently remembered versus forgotten items or pairs. Age deficits in successful encoding activity in hippocampal and prefrontal regions were more pronounced for SM (pairs) as compared with item memory (faces and scenes). Age-related reductions were also found in regions specialized in processing faces (fusiform face area) and scenes (parahippocampal place area), but these reductions were similar for item and SM. Functional connectivity between the hippocampus and the rest of the brain was also affected by aging; whereas connections with posterior cortices were weaker in older adults, connections with anterior cortices, including prefrontal regions, were stronger in older adults. Taken together, the results provide a link between SM deficits in older adults and reduced recruitment of hippocampal and prefrontal regions during encoding. The functional connectivity findings are consistent with a posterior-anterior shift with aging previously reported in several cognitive domains and linked to functional compensation.     

Infants rapidly detect human faces in complex naturalistic visual scenes

Infants respond preferentially to faces and face‐like stimuli from birth, but past research has typically presented faces in isolation or amongst an artificial array of competing objects. In the current study infants aged 3‐ to 12‐months viewed a series of complex visual scenes; half of the scenes contained a person, the other half did not. Infants rapidly detected and oriented to faces in scenes even when they were not visually salient. Although a clear developmental improvement was observed in face detection and interest, all infants displayed sensitivity to the presence of a person in a scene, by displaying eye movements that differed quantifiably across a range of measures when viewing scenes that either did or did not contain a person. We argue that infant's face detection capabilities are ostensibly “better” with naturalistic stimuli and artificial array presentations used in previous studies have underestimated performance.     

Early development of letter specialization in left fusiform is associated with better word reading and smaller fusiform face area

A functional region of left fusiform gyrus termed “the visual word form area” (VWFA) develops during reading acquisition to respond more strongly to printed words than to other visual stimuli. Here, we examined responses to letters among 5‐ and 6‐year‐old early kindergarten children (N = 48) with little or no school‐based reading instruction who varied in their reading ability. We used functional magnetic resonance imaging (fMRI) to measure responses to individual letters, false fonts, and faces in left and right fusiform gyri. We then evaluated whether signal change and size (spatial extent) of letter‐sensitive cortex (greater activation for letters versus faces) and letter‐specific cortex (greater activation for letters versus false fonts) in these regions related to (a) standardized measures of word‐reading ability and (b) signal change and size of face‐sensitive cortex (fusiform face area or FFA; greater activation for faces versus letters). Greater letter specificity, but not letter sensitivity, in left fusiform gyrus correlated positively with word reading scores. Across children, in the left fusiform gyrus, greater size of letter‐sensitive cortex correlated with lesser size of FFA. These findings are the first to suggest that in beginning readers, development of letter responsivity in left fusiform cortex is associated with both better reading ability and also a reduction of the size of left FFA that may result in right‐hemisphere dominance for face perception.     

Face detection in 2‐ to 6‐month‐old infants is influenced by gaze direction and species

Humans detect faces efficiently from a young age. Face detection is critical for infants to identify and learn from relevant social stimuli in their environments. Faces with eye contact are an especially salient stimulus, and attention to the eyes in infancy is linked to the emergence of later sociality. Despite the importance of both of these early social skills—attending to faces and attending to the eyes—surprisingly little is known about how they interact. We used eye tracking to explore whether eye contact influences infants' face detection. Longitudinally, we examined 2‐, 4‐, and 6‐month‐olds' (N = 65) visual scanning of complex image arrays with human and animal faces varying in eye contact and head orientation. Across all ages, infants displayed superior detection of faces with eye contact; however, this effect varied as a function of species and head orientation. Infants were more attentive to human than animal faces and were more sensitive to eye and head orientation for human faces compared to animal faces. Unexpectedly, human faces with both averted heads and eyes received the most attention. This pattern may reflect the early emergence of gaze following—the ability to look where another individual looks—which begins to develop around this age. Infants may be especially interested in averted gaze faces, providing early scaffolding for joint attention. This study represents the first investigation to document infants' attention patterns to faces systematically varying in their attentional states. Together, these findings suggest that infants develop early, specialized functional conspecific face detection.     

Biracial and monoracial infant own‐race face perception: an eye tracking study

We know that early experience plays a crucial role in the development of face processing, but we know little about how infants learn to distinguish faces from different races, especially for non‐Caucasian populations. Moreover, it is unknown whether differential processing of different race faces observed in typically studied monoracial infants extends to biracial infants as well. Thus, we investigated 3‐month‐old Caucasian, Asian and biracial (Caucasian‐Asian) infants’ ability to distinguish Caucasian and Asian faces. Infants completed two within‐subject, infant‐controlled habituation sequences and test trials as an eye tracker recorded looking times and scanning patterns. Examination of individual differences revealed significant positive correlations between own‐race novelty preference and scanning frequency between eye and mouth regions of own‐race habituation stimuli for Caucasian and Asian infants, suggesting that facility in own‐race face discrimination stems from active inspection of internal facial features in these groups. Biracial infants, however, showed the opposite effect: An ‘own‐race’ novelty preference was associated with reduced scanning between eye and mouth regions of ‘own‐race’ habituation stimuli, suggesting that biracial infants use a distinct approach to processing frequently encountered faces. Future directions for investigating face processing development in biracial populations are discussed. A video abstract of this article can be viewed at http://youtu.be/a_dDXfFuEfY     

Auditory evoked responses recorded from 16-month-old human infants to words they did and did not know

Auditory evoked responses (AERs) were recorded from the frontal, temporal, and parietal scalp regions of nine male and nine female 16-month-old infants while they listened to a series of words. The brain responses reliably discriminated between words the infants were thought to understand versus those that they did not appear to know as judged by their parents and two independent raters. Findings from this study indicated that the brain wave patterns could discriminate known from unknown words. Sex differences in the patterns of lateralized hemispheric responses to the known and unknown words were also noted. These data indicate that auditory evoked responses may be used to detect differences in word meanings in young infants.     

Domain‐specific development of face memory but not face perception

How does the remarkable human ability for face recognition arise over development? Competing theories have proposed either late maturity (beyond 10 years) or early maturity (before 5 years), but have not distinguished between perceptual and memory aspects of face recognition. Here, we demonstrate a perception–memory dissociation. We compare rate of development for (adult, human) faces versus other social stimuli (bodies), other discrete objects (cars), and other categories processed in discrete brain regions (scenes, bodies), from 5 years to adulthood. For perceptual discrimination, performance improved with age at the same rate for faces and all other categories, indicating no domain‐specific development. In contrast, face memory increased more strongly than non‐face memory, indicating domain‐specific development. The results imply that each theory is partly true: the late maturity theory holds for face memory, and the early maturity theory for face perception.     

Neural correlates of facial emotion processing in infancy

In the present study we examined the neural correlates of facial emotion processing in the first year of life using ERP measures and cortical source analysis. EEG data were collected cross‐sectionally from 5‐ (N = 49), 7‐ (N = 50), and 12‐month‐old (N = 51) infants while they were viewing images of angry, fearful, and happy faces. The N290 component was found to be larger in amplitude in response to fearful and happy than angry faces in all posterior clusters and showed largest response to fear than the other two emotions only over the right occipital area. The P400 and Nc components were found to be larger in amplitude in response to angry than happy and fearful faces over central and frontal scalp. Cortical source analysis of the N290 component revealed greater cortical activation in the right fusiform face area in response to fearful faces. This effect started to emerge at 5 months and became well established at 7 months, but it disappeared at 12 months. The P400 and Nc components were primarily localized to the PCC/Precuneus where heightened responses to angry faces were observed. The current results suggest the detection of a fearful face in infants’ brain can happen shortly (~200–290 ms) after the stimulus onset, and this process may rely on the face network and develop substantially between 5 to 7 months of age. The current findings also suggest the differential processing of angry faces occurred later in the P400/Nc time window, which recruits the PCC/Precuneus and is associated with the allocation of infants’ attention.     

Exploring cortical activation and connectivity in infants with and without familial risk for autism during naturalistic social interactions: A preliminary study

Behavioral signs of Autism Spectrum Disorder (ASD) are typically observable by the second year of life and a reliable diagnosis of ASD is possible by 2 to 3 years of age. Studying infants with familial risk for ASD allows for the investigation of early signs of ASD risk within the first year. Brain abnormalities such as hyper-connectivity within the first year may precede the overt signs of ASD that emerge later in life. In this preliminary study, we use functional near-infrared spectroscopy (fNIRS), an infant-friendly neuroimaging tool that is relatively robust against motion artifacts, to examine functional activation and connectivity during naturalistic social interactions in 9 high-risk (HR; older sibling with ASD) and 6 low-risk (LR; no family history of ASD) infants from 6 to 9 months of age. We obtained two 30-second baseline periods and a 5-minute social interaction period. HR infants showed reduced right and left-hemispheric activation compared to LR infants based on oxy (HbO₂) and deoxy (HHb) signal trends. HR infants also had greater functional connectivity than LR infants during the pre- and post-social periods and showed a drop in connectivity during the social period. Our findings are consistent with previous work suggesting early differences in cortical activation associated with familial risk for ASD, and highlight the promise of fNIRS in evaluating potential markers of ASD risk during naturalistic social contexts.     

Shedding light on words and sentences: near-infrared spectroscopy in language research

Investigating the neuronal network underlying language processing may contribute to a better understanding of how the brain masters this complex cognitive function with surprising ease and how language is acquired at a fast pace in infancy. Modern neuroimaging methods permit to visualize the evolvement and the function of the language network. The present paper focuses on a specific methodology, functional near-infrared spectroscopy (fNIRS), providing an overview over studies on auditory language processing and acquisition. The methodology detects oxygenation changes elicited by functional activation of the cerebral cortex. The main advantages for research on auditory language processing and its development during infancy are an undemanding application, the lack of instrumental noise, and its potential to simultaneously register electrophysiological responses. Also it constitutes an innovative approach for studying developmental issues in infants and children. The review will focus on studies on word and sentence processing including research in infants and adults.     

Infant preference for female faces occurs for same‐ but not other‐race faces

There has been a recent surge of interest in the question of how infants respond to the social attributes of race and gender information in faces. This work has demonstrated that by 3 months of age, infants will respond preferentially to same‐race faces and faces depicting the gender of the primary caregiver. In the current study, we investigated emergence of the female face preference for same‐ versus other‐race faces to examine whether the determinants of preference for face gender and race are independent or interactive in young infants. In Expt 1, 3‐month‐old Caucasian infants displayed a preference for female over male faces when the faces were Caucasian, but not when the faces were Asian. In Expt 2, new‐born Caucasian infants did not demonstrate a preference for female over male faces for Caucasian faces. The results are discussed in terms of a face prototype that becomes progressively tuned as it is structured by the interaction of the gender and race of faces that are experienced during early development.     

The neural correlates of orienting to walking direction in 6‐month‐old infants: An ERP study

The ability to detect social signals represents a first step to enter our social world. Behavioral evidence has demonstrated that 6‐month‐old infants are able to orient their attention toward the position indicated by walking direction, showing faster orienting responses toward stimuli cued by the direction of motion than toward uncued stimuli. The present study investigated the neural mechanisms underpinning this attentional priming effect by using a spatial cueing paradigm and recording EEG (Geodesic System 128 channels) from 6‐month‐old infants. Infants were presented with a central point‐light walker followed by a single peripheral target. The target appeared randomly at a position either congruent or incongruent with the walking direction of the cue. We examined infants' target‐locked event‐related potential (ERP) responses and we used cortical source analysis to explore which brain regions gave rise to the ERP responses. The P1 component and saccade latencies toward the peripheral target were modulated by the congruency between the walking direction of the cue and the position of the target. Infants' saccade latencies were faster in response to targets appearing at congruent spatial locations. The P1 component was larger in response to congruent than to incongruent targets and a similar congruency effect was found with cortical source analysis in the parahippocampal gyrus and the anterior fusiform gyrus. Overall, these findings suggest that a type of biological motion like the one of a vertebrate walking on the legs can trigger covert orienting of attention in 6‐month‐old infants, enabling enhancement of neural activity related to visual processing of potentially relevant information as well as a facilitation of oculomotor responses to stimuli appearing at the attended location.     

Using innate visual biases to guide face learning in natural scenes: a computational investigation

Newborn infants appear to possess an innate bias that guides preferential orienting to and tracking of human faces. There is, however, no clear agreement as to the underlying mechanism supporting such a preference. In particular, two competing theories (known as the ‘structural’ and ‘sensory’ hypotheses) conjecture fundamentally different biasing mechanisms to explain this behavior. The structural hypothesis suggests that a crude ‘3‐dot’ representation of face‐specific geometry is responsible for the exhibited preference. By contrast, the sensory hypothesis suggests that face preference is the product of several generic visual preferences for qualities like dark/light vertical asymmetry, horizontal symmetry, and high contrast. To complement existing empirical results, the current study describes a computational investigation of how well both proposals actually support face detection in cluttered natural scenes. The results demonstrate that both models are capable of locating faces effectively, but that the model suggested by the ‘sensory hypothesis’ is more selective than the model suggested by the ‘structural hypothesis’.     

Perceptual narrowing towards adult faces is a cross‐cultural phenomenon in infancy: a behavioral and near‐infrared spectroscopy study with Japanese infants

Recent data showed that, in Caucasian infants, perceptual narrowing occurs for own‐race adult faces between 3 and 9 months of age, possibly as a consequence of the extensive amount of social and perceptual experience accumulated with caregivers and/or other adult individuals of the same race of the caregiver. The neural correlates of this developmental process remain unexplored, and it is currently unknown whether perceptual tuning towards adult faces can be extended to other cultures. To this end, in the current study we tested the ability of 3‐ and 9‐month‐old Japanese infants to discriminate among adult and infant Asian faces in a visual familiarization task (Experiment 1), and compared 9‐month‐olds’ cerebral hemodynamic responses to adult and infant faces as measured by near‐infrared spectroscopy (NIRS) (Experiment 2). Results showed that 3‐month‐olds exhibit above‐chance discrimination of adult and infant faces, whereas 9‐month‐olds discriminate adult faces but not infant faces (Experiment 1). Moreover, adult faces, but not infant faces, induced significant increases in hemodynamic responses in the right temporal areas of 9‐month‐old infants. Overall, our data suggest that perceptual narrowing towards adult faces is a cross‐cultural phenomenon occurring between 3 and 9 months of age, and translates by 9 months of age into a right‐hemispheric specialization in the processing of adult faces.     

Asymmetrical cortical processing of radial expansion / contraction in infants and adults

We report asymmetrical cortical responses (steady‐state visual evoked potentials) to radial expansion and contraction in human infants and adults. Forty‐four infants (22 3‐month‐olds and 22 4‐month‐olds) and nine adults viewed dynamic dot patterns which cyclically (2.1 Hz) alternate between radial expansion (or contraction) and random directional motion. The first harmonic (F1) response in the steady‐state VEP response must arise from mechanisms sensitive to the global radial motion structure. We compared F1 amplitudes between expansion‐random and contraction‐random motion alternations. F1 amplitudes for contraction were significantly larger than those for expansion for the older infants and adults but not for the younger infants. These results suggest that the human cortical motion mechanisms have asymmetrical sensitivity for radial expansion vs. contraction, which develops at around 4 months of age. The relation between development of sensitivity to radial motion and cortical motion mechanisms is discussed.     

Neural correlates of perceptual narrowing in cross‐species face‐voice matching

Integrating the multisensory features of talking faces is critical to learning and extracting coherent meaning from social signals. While we know much about the development of these capacities at the behavioral level, we know very little about the underlying neural processes. One prominent behavioral milestone of these capacities is the perceptual narrowing of face–voice matching, whereby young infants match faces and voices across species, but older infants do not. In the present study, we provide neurophysiological evidence for developmental decline in cross‐species face–voice matching. We measured event‐related brain potentials (ERPs) while 4‐ and 8‐month‐old infants watched and listened to congruent and incongruent audio‐visual presentations of monkey vocalizations and humans mimicking monkey vocalizations. The ERP results indicated that younger infants distinguished between the congruent and the incongruent faces and voices regardless of species, whereas in older infants, the sensitivity to multisensory congruency was limited to the human face and voice. Furthermore, with development, visual and frontal brain processes and their functional connectivity became more sensitive to the congruence of human faces and voices relative to monkey faces and voices. Our data show the neural correlates of perceptual narrowing in face–voice matching and support the notion that postnatal experience with species identity is associated with neural changes in multisensory processing ( Lewkowicz & Ghazanfar, 2009 ).     

婴幼儿面孔注意偏向：先天倾向与发展轨迹——来自正常和孤独症婴幼儿的证据

正常发展(Typically developing, TD)婴儿的先天面孔注意倾向稳定地存在于不同发展阶段不同刺激情景中, 且在生命第一年内呈现短暂下降后快速增强的发展趋势。TD婴幼儿的视觉注意在第4至6周之间发生由皮下控制向皮层控制的关键性转变之后, 伴随面孔视觉经验的不断积累, 逐渐形成的面孔特异性皮层网络对面孔的优先选择性反应逐渐增强。而孤独症谱系(Autism Spectrum Disorder, ASD)婴幼儿具备初始的面孔注意先天倾向, 但在面孔皮层发育关键期内逐渐偏离正常轨道, 在1岁左右表现出面孔注意障碍。该群体先天的感知注意损伤或社会动机缺失可能导致其在关键性转变期内的面孔视觉经验输入不足, 进而阻碍面孔特异性皮层网络的正常发展。未来研究可考虑采用生物遗传学方法和近红外脑成像技术探索新生儿面孔注意先天倾向的起源, 系统考察社会场景中感知觉特征和社会性特征对ASD高危婴儿面孔注意发展轨迹尤其是关键性转变期的影响作用。