Developmental changes in neural lateralization for visual-spatial function: Evidence from a line-bisection task.

Studies of hemispheric specialization have traditionally cast the left hemisphere as specialized for language and the right hemisphere for spatial function. Much of the supporting evidence for this separation of function comes from studies of healthy adults and those who have sustained lesions to the right or left hemisphere. However, we know little about the developmental origins of lateralization. Recent evidence suggests that the young brain represents language bilaterally, with 4-6-year-olds activating the left-hemisphere regions known to support language in adults as well as homotopic regions in the right hemisphere. This bilateral pattern changes over development, converging on left-hemispheric activation in late childhood. In the present study, we ask whether this same developmental trajectory is observed in a spatial task that is strongly right-lateralized in adults-the line bisection (or "Landmark") task. We examined fMRI activation among children ages 5-11 years as they were asked to judge which end of a bisected vertical line was longer. We found that young children showed bilateral activation, with activation in the same areas of the right hemisphere as has been shown among adults, as well as in the left hemisphere homotopic regions. By age 10, activation was right-lateralized. This strongly resembles the developmental trajectory for language, moving from bilateral to lateralized activation. We discuss potential underlying mechanisms and suggest that understanding the development of lateralization for a range of cognitive functions can play a crucial role in understanding general principles of how and why the brain comes to lateralize certain functions.

Development of bilateral parietal activation for complex visual-spatial function: Evidence from a visual-spatial construction task.

The neural representation of visual-spatial functions has traditionally been ascribed to the right hemisphere, but little is known about these representations in children, including whether and how lateralization of function changes over the course of development. Some studies suggest bilateral activation early in life that develops toward right-lateralization in adulthood, while others find evidence of right-hemispheric dominance in both children and adults. We used a complex visual-spatial construction task to examine the nature of lateralization and its developmental time course in children ages 5-11 years. Participants were shown two puzzle pieces and were asked whether the pieces could fit together to make a square; responses required either mental translation of the pieces (Translation condition) or both mental translation and rotation of the pieces (Rotation condition). Both conditions were compared to a matched Luminance control condition that was similar in terms of visual content and difficulty but required no spatial analysis. Group and single-subject analyses revealed that the Rotation and Translation conditions elicited strongly bilateral activation in the same parietal and occipital locations as have been previously found for adults. These findings show that visual-spatial construction consistently elicits robust bilateral activation from age 5 through adulthood. This challenges the idea that spatial functions are all right-lateralized, either during early development or in adulthood. More generally, these findings provide insights into the developmental course of lateralization across different spatial skills and how this may be influenced by the computational requirements of the particular functions involved.

What you say versus how you say it: Comparing sentence comprehension and emotional prosody processing using fMRI.

While language processing is often described as lateralized to the left hemisphere (LH), the processing of emotion carried by vocal intonation is typically attributed to the right hemisphere (RH) and more specifically, to areas mirroring the LH language areas. However, the evidence base for this hypothesis is inconsistent, with some studies supporting right-lateralization but others favoring bilateral involvement in emotional prosody processing. Here we compared fMRI activations for an emotional prosody task with those for a sentence comprehension task in 20 neurologically healthy adults, quantifying lateralization using a lateralization index. We observed right-lateralized frontotemporal activations for emotional prosody that roughly mirrored the left-lateralized activations for sentence comprehension. In addition, emotional prosody also evoked bilateral activation in pars orbitalis (BA47), amygdala, and anterior insula. These findings are consistent with the idea that analysis of the auditory speech signal is split between the hemispheres, possibly according to their preferred temporal resolution, with the left preferentially encoding phonetic and the right encoding prosodic information. Once processed, emotional prosody information is fed to domain-general emotion processing areas and integrated with semantic information, resulting in additional bilateral activations.

Two rooms, two representations? Episodic-like memory in toddlers and preschoolers.

Episodic memory involves binding together what-where-when associations. In three experiments, we tested the development of memory for such contextual associations in a naturalistic setting. Children searched for toys in two rooms with two different experimenters; each room contained two identical sets of four containers, but arranged differently. A distinct toy was hidden in a distinct container in each room. In Experiment 1, which involved children between 15 and 26 months who were prompted with a very explicit cue (a part of the hidden toy), we found a marked shift in performance with age: while 15- to 20-month-olds concentrated their searches on the two containers that sometimes contained toys, they did not distinguish between them according to context, but 21-26-month-olds did. However, surprisingly, without toy cues, even the youngest children showed a fragile ability to disambiguate the two containers by room context. In Experiment 2, we tested 34- to 40-month-olds and 64- to 72-month-olds without toy cues. The 5-year-olds were nearly perfect, and the 3-year-olds showed a significant preference for the correct container given only the context. In Experiment 3, we filled in the age range, and also investigated the effects of the use of labels (i.e. names of experimenters and rooms) and of familiarization time, in groups of 34- to 40-month-olds, 42- to 48-month-olds, and 50- to 56-month-olds. Neither labels nor familiarization time had an effect. Across experiments, there was regular age-related improvement in context-based memory. Overall, the results suggest that children's episodic memory may undergo an early qualitative change, yet to be precisely characterized, and that continuing increments in the use of contextual cues occur throughout the preschool period. A video abstract of this article can be viewed at https://www.youtube.com/watch?v=DkwEFw0UEz4&list=PLwxXcOKHPC0llAPVcJyW4EtzlA934A2Rz&index=1.

Using a touch screen paradigm to assess the development of mental rotation between 3½ and 5½ years of age.

Mental rotation is an important spatial skill. However, there is controversy concerning its early development and susceptibility to intervention. In the present study, we assessed individual differences in the mental rotation abilities of children between 3½ and 5½ years of age, using a touch screen paradigm to simplify task demands. A figure or its mirror image was presented in 8 different orientations, and children indicated in which of two holes the figure would fit by touching one of the holes on the screen. Task instructions were varied in three conditions, giving the children the opportunity to gather manual or observational experience with rotations of different stimuli, or giving no additional experience. Children's error rates and response times increased linearly with increasing angular disparity between the figure and the hole by the age of 5 years, but 4-year-olds were found to respond at chance for all angular disparities, despite the use of a touch screen paradigm. Both manual and observational experience increased the response accuracy of 5-year-olds, especially for children already performing well. However, there was no effect on 4-year-olds. Results point to an emerging readiness to use mental rotation and profit from observational and manual experience at age 5.

Impaired behavioral and neural representation of scenes in Williams syndrome.

Boundaries are crucial to our representation of the geometric shape of scenes, which can be used to reorient in space. Behavioral research has shown that children and adults share exquisite sensitivity to a defining feature of a boundary: its vertical extent. Imaging studies have shown that this boundary property is represented in the parahippocampal place area (PPA) among typically developed (TD) adults. Here, we show that sensitivity to the vertical extent of scene boundaries is impaired at both the behavioral and neural level in people with Williams syndrome (WS), a genetic deficit that results in severely impaired spatial functions. Behavioral reorientation was tested in three boundary conditions: a flat Mat, a 5 cm high Curb, and full Walls. Adults with WS could reorient in a rectangular space defined by Wall boundaries, but not Curb or Mat boundaries. In contrast, TD age-matched controls could reorient by all three boundary types and TD 4-year-olds could reorient by either Wall or Curb boundaries. Using fMRI, we find that the WS behavioral deficit is echoed in their neural representation of boundaries. While TD age-matched controls showed distinct neural responses to scenes depicting Mat, Curb, and Wall boundaries in the PPA, people with WS showed only a distinction between the Wall and Mat or Curb, but no distinction between the Mat and Curb. Taken together, these results reveal a close coupling between the representation of boundaries as they are used in behavioral reorientation and neural encoding, suggesting that damage to this key element of spatial representation may have a genetic foundation.

Revisiting the Landmark Task as a tool for studying hemispheric specialization: What's really right?

The "Landmark Task" (LT) is a line bisection judgment task that predominantly activates right parietal cortex. The typical version requires observers to judge bisections for horizontal lines that cross their egocentric midline and therefore may depend on spatial attention as well as spatial representation of the line segments. To ask whether the LT is indeed right-lateralized regardless of spatial attention (for which the right hemisphere is known to be important), we examined LT activation in 26 neurologically healthy young adults using vertical (instead of horizontal) stimuli, as compared with a luminance control task that made similar demands on spatial attention. We also varied task difficulty, which is known to affect lateralization in both spatial and language tasks. Despite these changes to the task, we observed right-lateralized parietal activations similar to those reported in other LT studies, both at group level and in individual lateralization indices. We conclude that LT activation is robustly right-lateralized, perhaps uniquely so among commonly-studied spatial tasks. We speculate that the unique properties of the LT reside in its requirement to judge relative magnitudes of the two line segments, rather than in the more general aspects of spatial attention or visual-spatial representation.

Detailed Visual Memory Capacity Is Present Early in Childhood.

Previous studies have shown that adults are able to remember more than 1,000 images with great detail. However, little is known about the development of this visual capacity, nor its presence early in life. This study tests the level of detail of young children's memory for a large number of items, adapting the method of Brady, Konkle, Alvarez, and Oliva (2008). Four- and six-year-old children were shown more than 100 images of everyday objects. They were then tested for recognition of familiar items in a binary decision task. The identity of the foil test item was manipulated in three conditions (Category, Exemplar, and State). Children demonstrated high accuracy across all conditions, remembering not only the basic-level category (Category), but also unique details (Exemplar), and information about position and arrangement of parts (State). These findings demonstrate that children spontaneously encode a high degree of visual detail. Early in life, visual memory exhibits high fidelity and extends over a large set of items.

Bilateral parietal activations for complex visual-spatial functions: Evidence from a visual-spatial construction task.

In this paper, we examine brain lateralization patterns for a complex visual-spatial task commonly used to assess general spatial abilities. Although spatial abilities have classically been ascribed to the right hemisphere, evidence suggests that at least some tasks may be strongly bilateral. For example, while functional neuroimaging studies show right-lateralized activations for some spatial tasks (e.g., line bisection), bilateral activations are often reported for others, including classic spatial tasks such as mental rotation. Moreover, constructive apraxia has been reported following left- as well as right-hemisphere damage in adults, suggesting a role for the left hemisphere in spatial function. Here, we use functional neuroimaging to probe lateralization while healthy adults carry out a simplified visual-spatial construction task, in which they judge whether two geometric puzzle pieces can be combined to form a square. The task evokes strong bilateral activations, predominantly in parietal and lateral occipital cortex. Bilaterality was observed at the single-subject as well as at the group level, and regardless of whether specific items required mental rotation. We speculate that complex visual-spatial tasks may generally engage more bilateral activation of the brain than previously thought, and we discuss implications for understanding hemispheric specialization for spatial functions.

Neural representation of scene boundaries.

Three-dimensional environmental boundaries fundamentally define the limits of a given space. A body of research employing a variety of methods points to their importance as cues in navigation. However, little is known about the nature of the representation of scene boundaries by high-level scene cortices in the human brain (namely, the parahippocampal place area (PPA) and retrosplenial complex (RSC)). Here we use univariate and multivoxel pattern analysis to study classification performance for artificial scene images that vary in degree of vertical boundary structure (a flat 2D boundary, a very slight addition of 3D boundary, or full walls). Our findings present evidence that there are distinct neural components for representing two different aspects of boundaries: 1) acute sensitivity to the presence of grounded 3D vertical structure, represented by the PPA, and 2) whether a boundary introduces a significant impediment to the viewer's potential navigation within a space, represented by RSC.

Spatial Language and the Embedded Listener Model in Parents' Input to Children.

Language is a collaborative act: To communicate successfully, speakers must generate utterances that are not only semantically valid but also sensitive to the knowledge state of the listener. Such sensitivity could reflect the use of an "embedded listener model," where speakers choose utterances on the basis of an internal model of the listener's conceptual and linguistic knowledge. In this study, we ask whether parents' spatial descriptions incorporate an embedded listener model that reflects their children's understanding of spatial relations and spatial terms. Adults described the positions of targets in spatial arrays to their children or to the adult experimenter. Arrays were designed so that targets could not be identified unless spatial relationships within the array were encoded and described. Parents of 3-4-year-old children encoded relationships in ways that were well-matched to their children's level of spatial language. These encodings differed from those of the same relationships in speech to the adult experimenter (Experiment 1). In contrast, parents of individuals with severe spatial impairments (Williams syndrome) did not show clear evidence of sensitivity to their children's level of spatial language (Experiment 2). The results provide evidence for an embedded listener model in the domain of spatial language and indicate conditions under which the ability to model listener knowledge may be more challenging.

Geometric and featural systems, separable and combined: Evidence from reorientation in people with Williams syndrome.

Spatial reorientation by humans and other animals engages geometric representations of surface layouts as well as featural landmarks; however, the two types of information are thought to be behaviorally and neurally separable. In this paper, we examine the use of these two types of information during reorientation among children and adults with Williams syndrome (WS), a genetic disorder accompanied by abnormalities in brain regions that support use of both geometry and landmarks. Previous studies of reorientation in adolescents and adults with WS have shown deficits in the ability to use geometry for reorientation, but intact ability to use features, suggesting that the two systems can be differentially impaired by genetic disorder. Using a slightly modified layout, we found that many WS participants could use geometry, and most could use features along with geometry. However, the developmental trajectories for the two systems were quite different from one other, and different from those found in typical development. Purely geometric responding was not correlated with age in WS, and search processes appeared similar to those in typically developing (TD) children. In contrast, use of features in combination with geometry was correlated with age in WS, and search processes were distinctly different from TD children. The results support the view that use of geometry and features stem from different underlying mechanisms, that the developmental trajectories and operation of each are altered in WS, and that combination of information from the two systems is atypical. Given brain abnormalities in regions supporting the two kinds of information, our findings suggest that the co-operation of the two systems is functionally altered in this genetic syndrome.

Space and language in Williams syndrome: insights from typical development.

One of the holy grails of cognitive science is to understand the causal chain that links genes and cognition. Genetic syndromes accompanied by cognitive effects offer natural experiments that can uniquely inform our understanding of this chain. In this article, we discuss the case of Williams syndrome (WS), which is characterized by a set of missing genes on chromosome 7q11.23, and presents with a unique cognitive profile that includes severe spatial impairment along with strikingly fluent and well-structured language. An early inference from this profile was the idea that a small group of genes could directly target one cognitive system while leaving others unaffected. Recent evidence shows that this inference fails. First, the profile within the spatial domain is varied, with relative strength in some aspects of spatial representation but severe impairment in others. Second, some aspects of language may fail to develop fully, raising the question of how to compare the resilience and fragility of the two key cognitive domains in this syndrome. Third, much research on the profile fails to place findings in the context of typical developmental trajectories. We explore these points and propose a new hypothesis that explains the unusual WS cognitive profile by considering normal mechanisms of cognitive development that undergo change on an extremely prolonged timetable. This hypothesis places the elements of the WS cognitive profile in a new light, refocuses the discussion of the gene-cognition causal chain for WS and other disorders, and more generally, underlines the importance of understanding cognitive structure in both typical and atypical development. WIREs Cogn Sci 2013, 4:693-703. doi: 10.1002/wcs.1258 Conflict of interest: The authors have declared no conflicts of interest for this article. For further resources related to this article, please visit the WIREs website.