Face and location processing in children with early unilateral brain injury.

Human visuospatial functions are commonly divided into those dependent on the ventral visual stream (ventral occipitotemporal regions), which allows for processing the 'what' of an object, and the dorsal visual stream (dorsal occipitoparietal regions), which allows for processing 'where' an object is in space. Information about the development of each of the two streams has been accumulating, but very little is known about the effects of injury, particularly very early injury, on this developmental process. Using a set of computerized dorsal and ventral stream tasks matched for stimuli, required response, and difficulty (for typically-developing individuals), we sought to compare the differential effects of injury to the two systems by examining performance in individuals with perinatal brain injury (PBI), who present with selective deficits in visuospatial processing from a young age. Thirty participants (mean=15.1 years) with early unilateral brain injury (15 right hemisphere PBI, 15 left hemisphere PBI) and 16 matched controls participated. On our tasks children with PBI performed more poorly than controls (lower accuracy and longer response times), and this was particularly prominent for the ventral stream task. Lateralization of PBI was also a factor, as the dorsal stream task did not seem to be associated with lateralized deficits, with both PBI groups showing only subtle decrements in performance, while the ventral stream task elicited deficits from RPBI children that do not appear to improve with age. Our findings suggest that early injury results in lesion-specific visuospatial deficits that persist into adolescence. Further, as the stimuli used in our ventral stream task were faces, our findings are consistent with what is known about the neural systems for face processing, namely, that they are established relatively early, follow a comparatively rapid developmental trajectory (conferring a vulnerability to early insult), and are biased toward the right hemisphere.

The effects of injury to dynamic neural networks in the mature and developing brain.

This special section emphasizes three key factors relevant to understanding brain responses to injury. First, it is important to consider the impact of injury on brain networks rather then just the localized neuropathology. In contrast to older localizationist models, neural systems views emphasize that the effects of localized injury cascade through the neural system altering function at multiple levels. Thus, effective remediation must accommodate the multiple effects of brain injury. Second, the role of neural plasticity in the brain response to injury is critical. Rehabilitation implies that neural system is adaptive and capable of changing in response to input. Thus exploiting the brain's inherent plasticity is central to remediation. Finally, the timing of injury is an essential consideration. Adult injury disrupts stable neural systems and plasticity operates to regain functional balance. In contrast, early injury affects fundamental development processes and alters the emerging organization and functioning of neural systems.

The basics of brain development.

Over the past several decades, significant advances have been made in our understanding of the basic stages and mechanisms of mammalian brain development. Studies elucidating the neurobiology of brain development span the levels of neural organization from the macroanatomic, to the cellular, to the molecular. Together this large body of work provides a picture of brain development as the product of a complex series of dynamic and adaptive processes operating within a highly constrained, genetically organized but constantly changing context. The view of brain development that has emerged from the developmental neurobiology literature presents both challenges and opportunities to psychologists seeking to understand the fundamental processes that underlie social and cognitive development, and the neural systems that mediate them. This chapter is intended to provide an overview of some very basic principles of brain development, drawn from contemporary developmental neurobiology, that may be of use to investigators from a wide range of disciplines.

Hierarchical forms processing in adults and children.

Two experiments examined child and adult processing of hierarchical stimuli composed of geometric forms. Adults (ages 18-23 years) and children (ages 7-10 years) performed a forced-choice task gauging similarity between visual stimuli consisting of large geometric objects (global level) composed of small geometric objects (local level). The stimuli spatial arrangement was manipulated to assess child and adult reaction times and predisposition toward local or global form categorization under two distinct trial conditions, with varied density of the local forms comprising the global forms. In Experiment 1, children and adults were presented with common, simple geometric shape hierarchical forms composed of ovals and rectangles. In Experiment 2, adults were presented with hierarchical forms composed of the simple geometric shapes, ovals and rectangles, and additional novel complex geometric shapes, "posts" and "arches." Results show a clear increase of global processing bias across the age ranges of the individuals in the study, with children at 10 years performing similarly to adults on the simple stimuli. In addition, adults presented with the novel complex geometric shapes showed a significant reduction in global processing bias, indicating that form novelty and complexity lead to additional attention to local features in categorization tasks.

Effects of early focal brain injury on memory for visuospatial patterns: selective deficits of global-local processing.

Selective deficits in visuospatial processing are present early in development among children with perinatal focal brain lesions (PL). Children with right hemisphere PL (RPL) are impaired in configural processing, while children with left hemisphere PL (LPL) are impaired in featural processing. Deficits associated with LPL are less pervasive than those observed with RPL, but this difference may reflect the structure of the tasks used for assessment. Many of the tasks used to date may place greater demands on configural processing, thus highlighting this deficit in the RPL group. This study employed a task designed to place comparable demands on configural and featural processing, providing the opportunity to obtain within-task evidence of differential deficit. Sixty-two 5- to 14-year-old children (19 RPL, 19 LPL, and 24 matched controls) reproduced from memory a series of hierarchical forms (large forms composed of small forms). Global- and local-level reproduction accuracy was scored. Controls were equally accurate on global- and local-level reproduction. Children with RPL were selectively impaired on global accuracy, and children with LPL on local accuracy, thus documenting a double dissociation in global-local processing.

Principles of brain development.

Throughout much of the 20th century, the major models of brain development were strongly deterministic. It was thought that brain development proceeds via a prescribed blueprint that is somehow innately specified in the organism. Contemporary models present a distinctly different view of both inheritance and brain development. First, we do not inherit blueprints or plans, we inherit genes and the cellular machinery for expressing them. Genes carry essential information for creating proteins, but do not determine biological processes or developmental outcomes; the first cells contain the elements necessary for creating proteins based on the information coded in the nucleotide sequences of genes. Second, brain development is dynamic: the biological state of the brain at any moment is the product of developmental processes that involve an intricate interplay among genes and an ever-expanding range of environmental factors-from local cellular events to influences from the outside world. In science, models matter. They reflect underlying assumptions about how things can happen, and thus influence the kinds of questions we ask, the kinds of experiments we propose, the therapies we develop, and the educational curricula we construct. The dynamic model of brain development accounts for powerful neurobehavioral effects that can simply not be accommodated by deterministic models. WIREs Cogn Sci 2017, 8:e1402. doi: 10.1002/wcs.1402 For further resources related to this article, please visit the WIREs website.

Construction of the human forebrain.

The adult human brain is arguably the most complex of biological systems. It contains 86 billion neurons (the information processing cells of the brain) and many more support cells. The neurons, with the assistance of the support cells, form trillions of connections creating complex, interconnected neural networks that support all human thought, feeling, and action. A challenge for modern neuroscience is to provide a model that accounts for this exquisitely complex and dynamic system. One fundamental part of this model is an account of how the human brain develops. This essay describes two important aspects of this developmental story. The first part of the story focuses on the remarkable and dynamic set of events that unfold during the prenatal period to give rise to cell lineage that form the essential substance of the brain, particularly the structures of the cerebral hemispheres. The second part of the story focuses on the formation of the major brain pathways of the cerebrum, the intricate fiber bundles that connect different populations of neurons to form the information processing systems that support all human thought and action. These two aspects of early brain development provide an essential foundation for understanding how the structure, organization, and functioning of the human brain emerge. WIREs Cogn Sci 2017, 8:e1409. doi: 10.1002/wcs.1409 For further resources related to this article, please visit the WIREs website.

Cognitive development following early brain injury: evidence for neural adaptation.

Over the past few decades a large body of work from developmental neurobiology has shown that mammalian brain development is the product of dynamic and adaptive processes operating within highly constrained, but continually changing, biological and environmental contexts. The recent study of children with prenatal focal brain injury supports this dynamic view of development for humans. Children's injuries often affect substantial portions of one cerebral hemisphere, resulting in damage that would compromise cognitive ability in adults. However, longitudinal behavioral studies of this population have revealed only mild deficits. It is suggested here that children's capacity for adaptation reflects normal developmental processes operating against a backdrop of serious neural perturbation. Data from three behavioral domains--linguistics, spatial cognition and affective development--illustrate this complex profile of change.

Hemispheric specialization for categorical and coordinate spatial relations during an image generation task: evidence from children and adults.

Hemispheric specialization of categorical and coordinate image generation was assessed in adults, 8-year-old and 10-year-old children. In a standardized image generation task, participants decided whether probes, presented in a blank grid (categorical task) or bracketed square (coordinate task), would have appeared on a previously studied letter. To ensure that participants mentally generated the target letter, probe location was varied. "Early" probes appeared on letter segments that are first produced when the letter is drawn; while "late" probes appeared on later produced segments. Like previous adult studies, the grid task elicited a left hemisphere "categorical" strategy; while the bracket task elicits a right hemisphere "coordinate" strategy. However, contrary to previous research, the results reveal the significant and complex effects of probe location on categorical and coordinate image generation abilities. Specifically, early probes elicited a strong right hemisphere advantage for both tasks across all ages, whereas late probes produced a left hemisphere dissociation between categorical and coordinate processing. The left hemisphere dissociation was evident only for 10-year-olds and adults, suggesting that younger children are not yet proficient in generating spatial representations.

How 'generalized' is the 'slowed processing' in SLI? The case of visuospatial attentional orienting.

The study was designed to assess the speed and efficiency of visuospatial attentional orienting and the speed of visual processing and motor response in school-age children diagnosed with specific language impairment (SLI). Fifteen participants with SLI (7-15 years old) and their gender- and age-matched normally developing peers performed two formats of a simple visual discrimination task, one requiring the use of attentional orienting for accurate performance, and the other not requiring shifts of attention. The SLI group was characterized by (a) slower visual processing, and (b) slower motor response, but (c) similar attentional orienting speed, relative to the control group. The results are discussed in relation to the 'generalized slowing hypothesis' in SLI and the neural underpinning of visuospatial attentional orienting and SLI.

The impact of early unilateral brain injury on perceptual organization and visual memory.

Studies of young children with early unilateral brain injury have suggested that while hemispheric differences in visuospatial processing appear to be present early in development, the young brain is better able to compensate for injury than when the injury occurs later, after networks have been established. The aim of this study was to determine if this pattern continues later in development when these children are given a challenging task: the Rey-Osterrieth Complex Figure. Experiment 1 included longitudinal data from ten children with early left hemisphere (LH) injury and nine children with early right hemisphere (RH) injury. Injury was presumed to be due to a prenatal or perinatal stroke. Compared with typically developing children, both groups were poorer in copying the figure. With development, these children produced reasonably accurate drawings but continued to use the most immature and piecemeal strategy. In Experiment 2, copy and immediate memory drawings from the 19 children with early unilateral brain injury were collected at a single age (11-14 years). Eight of the ten children with LH injury organized their memory reproductions around the core rectangle but included relatively few additional details. In contrast, only two of the nine children with RH injury organized their memory reproductions around the core rectangle and all but one produced the figure in a piecemeal manner. The results from both studies demonstrate the continuation of subtle deficits in visuospatial analysis with development but also the continued capacity for compensation.

Face and place processing in Williams syndrome: evidence for a dorsal-ventral dissociation.

Individuals with Williams syndrome (WMS) show an interesting dissociation of ability within the visuospatial domain, particularly between face perception and other visuospatial tasks. In this population, using tasks matched for stimuli, required response, and difficulty (for controls) is critical when comparing performance across these areas. We compared WMS individuals with a sample of typically developing 8- and 9-year-old children, and with a sample of adults, closer to the WMS participants in chronological age, in order to investigate performance across two precisely matched perceptual tasks, one assessing face processing and the other assessing proficiency in processing stimuli location. The pattern of performance seen in WMS, but not in controls, implicates a specific deficit of dorsal stream functioning in this syndrome.

Exploring developmental change in the neural bases of higher cognitive functions: the promise of functional magnetic resonance imaging.

The dramatic changes in cognitive ability observed throughout childhood mirror comparably significant changes in the developing brain. Studies of animals provide important data on associations between the development of behavior and the neural substrate. However, understanding the development of brain-behavior relations for higher cognitive functions in humans requires direct, concurrent measurement of behavior and brain functions in the children themselves. To date, such data have been very limited. Recent developments in functional magnetic resonance imaging (fMRI) provide the opportunity to systematically explore the development of brain-behavior relations in children. In this article we consider the potential of fMRI to contribute to researchers' understanding of the development of brain-behavior relations. We begin with an overview of the basic imaging method. We then review work from our own laboratory that demonstrates systematic patterns of association between performance on visuospatial tasks and patterns of brain activation, and we compare our findings with those from other laboratories focused on other cognitive domains. Finally, we discuss the potential impact of functional imaging on researchers' understanding of core issues in cognitive and brain development.

The functional architecture for face-processing expertise: FMRI evidence of the developmental trajectory of the core and the extended face systems.

Expertise in processing faces is a cornerstone of human social interaction. However, the developmental course of many key brain regions supporting face preferential processing in the human brain remains undefined. Here, we present findings from an FMRI study using a simple viewing paradigm of faces and objects in a continuous age sample covering the age range from 6 years through adulthood. These findings are the first to use such a sample paired with whole-brain FMRI analyses to investigate development within the core and extended face networks across the developmental spectrum from middle childhood to adulthood. We found evidence, albeit modest, for a developmental trend in the volume of the right fusiform face area (rFFA) but no developmental change in the intensity of activation. From a spatial perspective, the middle portion of the right fusiform gyrus most commonly found in adult studies of face processing was increasingly likely to be included in the FFA as age increased to adulthood. Outside of the FFA, the most striking finding was that children hyperactivated nearly every aspect of the extended face system relative to adults, including the amygdala, anterior temporal pole, insula, inferior frontal gyrus, anterior cingulate gyrus, and parietal cortex. Overall, the findings suggest that development is best characterized by increasing modulation of face-sensitive regions throughout the brain to engage only those systems necessary for task requirements.

Brain development and the nature versus nurture debate.

Over the past three decades, developmental neurobiologists have made tremendous progress in defining basic principles of brain development. This work has changed the way we think about how brains develop. Thirty years ago, the dominant model was strongly deterministic. The relationship between brain and behavioral development was viewed as unidirectional; that is, brain maturation enables behavioral development. The advent of modern neurobiological methods has provided overwhelming evidence that it is the interaction of genetic factors and the experience of the individual that guides and supports brain development. Brains do not develop normally in the absence of critical genetic signaling, and they do not develop normally in the absence of essential environmental input. The fundamental facts about brain development should be of critical importance to neuropsychologists trying to understand the relationship between brain and behavioral development. However, the underlying assumptions of most contemporary psychological models reflect largely outdated ideas about how the biological system develops and what it means for something to be innate. Thus, contemporary models of brain development challenge the foundational constructs of the nature versus nurture formulation in psychology. The key to understanding the origins and emergence of both the brain and behavior lies in understanding how inherited and environmental factors are engaged in the dynamic and interactive processes that define and guide development of the neurobehavioral system.

Postnatal brain development: structural imaging of dynamic neurodevelopmental processes.

After birth, there is striking biological and functional development of the brain's fiber tracts as well as remodeling of cortical and subcortical structures. Behavioral development in children involves a complex and dynamic set of genetically guided processes by which neural structures interact constantly with the environment. This is a protracted process, beginning in the third week of gestation and continuing into early adulthood. Reviewed here are studies using structural imaging techniques, with a special focus on diffusion weighted imaging, describing age-related brain maturational changes in children and adolescents, as well as studies that link these changes to behavioral differences. Finally, we discuss evidence for effects on the brain of several factors that may play a role in mediating these brain-behavior associations in children, including genetic variation, behavioral interventions, and hormonal variation associated with puberty. At present longitudinal studies are few, and we do not yet know how variability in individual trajectories of biological development in specific neural systems map onto similar variability in behavioral trajectories.

Individuating faces and common objects produces equal responses in putative face-processing areas in the ventral occipitotemporal cortex.

Controversy surrounds the proposal that specific human cortical regions in the ventral occipitotemporal cortex, commonly called the fusiform face area (FFA) and occipital face area (OFA), are specialized for face processing. Here, we present findings from an fMRI study of identity discrimination of faces and objects that demonstrates the FFA and OFA are equally responsive to processing stimuli at the level of individuals (i.e., individuation), be they human faces or non-face objects. The FFA and OFA were defined via a passive viewing task as regions that produced greater activation to faces relative to non-face stimuli within the middle fusiform gyrus and inferior occipital gyrus. In the individuation task, participants judged whether sequentially presented images of faces, diverse objects, or wristwatches depicted the identical or a different exemplar. All three stimulus types produced equivalent BOLD activation within the FFA and OFA; that is, there was no face-specific or face-preferential processing. Critically, individuation processing did not eliminate an object superiority effect relative to faces within a region more closely linked to object processing in the lateral occipital complex (LOC), suggesting that individuation processes are reasonably specific to the FFA and OFA. Taken together, these findings challenge the prevailing view that the FFA and OFA are face-specific processing regions, demonstrating instead that they function to individuate - i.e., identify specific individuals - within a category. These findings have significant implications for understanding the function of brain regions widely believed to play an important role in social cognition.

Amygdala response to faces parallels social behavior in Williams syndrome.

Individuals with Williams syndrome (WS), a genetically determined disorder, show relatively strong face-processing abilities despite poor visuospatial skills and depressed intellectual function. Interestingly, beginning early in childhood they also show an unusually high level of interest in face-to-face social interaction. We employed functional magnetic resonance imaging (fMRI) to investigate physiological responses in face-sensitive brain regions, including ventral occipito-temporal cortex and the amygdala, in this unique genetic disorder. Participants included 17 individuals with WS, 17 age- and gender-matched healthy adults (chronological age-matched controls, CA) and 17 typically developing 8- to 9-year-old children (developmental age controls, DA). While engaged in a face discrimination task, WS participants failed to recruit the amygdala, unlike both CA and DA controls. WS fMRI responses in ventral occipito-temporal cortex, however, were comparable to those of DA controls. Given the integral role of the amygdala in social behavior, the failure of WS participants to recruit this region during face processing may be a neural correlate of the abnormally high sociability that characterizes this disorder.

Perceptual organization and visual immediate memory in children with specific language impairment.

Children with specific language impairment (LI) have deficits on some nonverbal tasks, but it is not clear if these are related to specific visuospatial deficits or to more general deficits in processing strategies. Children with LI were given two visuospatial tasks that we have shown to be sensitive to strategy use as well as specific processing deficits. In Study 1, children with LI (N=29, ages 6 to 12 years) performed significantly worse than typically developing children (N=26) on the Hierarchical Forms Memory task. In Study 2, children with LI (N=15; ages 9 to 12 years) performed significantly worse than typically developing children (N=40) on the Rey-Osterrieth Complex Figure task. Children with LI were less accurate and tended to use a fairly piecemeal (immature) strategy when copying the figure and were less likely to draw the core rectangle in a more integrated fashion during the immediate memory condition. These results suggest children with LI have subtle deficits on visuospatial tasks that may be more indicative of limitations associated with processing load and planning than of specific visuospatial processing deficits.

The lesion methodology: contrasting views from adult and child studies.

A traditional approach for examining brain-behavior relations has been the lesion method. This method assumes a direct correspondence between the cognitive process compromised and the site of lesion. Historically, studies with adults have used this framework to map brain functions. In contrast, studies of children with early injury have addressed quite different issues. Developmental animal lesion studies and pediatric neuropsychology studies have focused on the level of plasticity exhibited following early injury. Resilency in behavioral development has suggested change in the underlying neural substrate. A new set of studies has applied converging, MRI-based methods to examine anatomical and functional development in intact brain regions following early injury and compared these data with behavioral outcomes on the same children. The findings reveal an interaction between early injury and normal mechanisms of development, which manifest as atypical behavioral, structural, and functional development.