Hemispheric functional organization, as revealed by naturalistic neuroimaging, in pediatric epilepsy patients with cortical resections.

Functional changes in the pediatric brain following neural injuries attest to remarkable feats of plasticity. Investigations of the neurobiological mechanisms that underlie this plasticity have largely focused on activation in the penumbra of the lesion or in contralesional, homotopic regions. Here, we adopt a whole-brain approach to evaluate the plasticity of the cortex in patients with large unilateral cortical resections due to drug-resistant childhood epilepsy. We compared the functional connectivity (FC) in patients' preserved hemisphere with the corresponding hemisphere of matched controls as they viewed and listened to a movie excerpt in a functional magnetic resonance imaging (fMRI) scanner. The preserved hemisphere was segmented into 180 and 200 parcels using two different anatomical atlases. We calculated all pairwise multivariate statistical dependencies between parcels, or parcel edges, and between 22 and 7 larger-scale functional networks, or network edges, aggregated from the smaller parcel edges. Both the left and right hemisphere-preserved patient groups had widespread reductions in FC relative to matched controls, particularly for within-network edges. A case series analysis further uncovered subclusters of patients with distinctive edgewise changes relative to controls, illustrating individual postoperative connectivity profiles. The large-scale differences in networks of the preserved hemisphere potentially reflect plasticity in the service of maintained and/or retained cognitive function.

A connectivity-constrained computational account of topographic organization in primate high-level visual cortex.

Inferotemporal (IT) cortex in humans and other primates is topographically organized, containing multiple hierarchically organized areas selective for particular domains, such as faces and scenes. This organization is commonly viewed in terms of evolved domain-specific visual mechanisms. Here, we develop an alternative, domain-general and developmental account of IT cortical organization. The account is instantiated in interactive topographic networks (ITNs), a class of computational models in which a hierarchy of model IT areas, subject to biologically plausible connectivity-based constraints, learns high-level visual representations optimized for multiple domains. We find that minimizing a wiring cost on spatially organized feedforward and lateral connections, alongside realistic constraints on the sign of neuronal connectivity within model IT, results in a hierarchical, topographic organization. This organization replicates a number of key properties of primate IT cortex, including the presence of domain-selective spatial clusters preferentially involved in the representation of faces, objects, and scenes; columnar responses across separate excitatory and inhibitory units; and generic spatial organization whereby the response correlation of pairs of units falls off with their distance. We thus argue that topographic domain selectivity is an emergent property of a visual system optimized to maximize behavioral performance under generic connectivity-based constraints.

With childhood hemispherectomy, one hemisphere can support-but is suboptimal for-word and face recognition.

The right and left cerebral hemispheres are important for face and word recognition, respectively-a specialization that emerges over human development. The question is whether this bilateral distribution is necessary or whether a single hemisphere, be it left or right, can support both face and word recognition. Here, face and word recognition accuracy in patients (median age 16.7 y) with a single hemisphere following childhood hemispherectomy was compared against matched typical controls. In experiment 1, participants viewed stimuli in central vision. Across both face and word tasks, accuracy of both left and right hemispherectomy patients, while significantly lower than controls' accuracy, averaged above 80% and did not differ from each other. To compare patients' single hemisphere more directly to one hemisphere of controls, in experiment 2, participants viewed stimuli in one visual field to constrain initial processing chiefly to a single (contralateral) hemisphere. Whereas controls had higher word accuracy when words were presented to the right than to the left visual field, there was no field/hemispheric difference for faces. In contrast, left and right hemispherectomy patients, again, showed comparable performance to one another on both face and word recognition, albeit significantly lower than controls. Altogether, the findings indicate that a single developing hemisphere, either left or right, may be sufficiently plastic for comparable representation of faces and words. However, perhaps due to increased competition or "neural crowding," constraining cortical representations to one hemisphere may collectively hamper face and word recognition, relative to that observed in typical development with two hemispheres.

A Possible Neural Basis for Attentional Capture of Faces Revealed by Functional Magnetic Resonance Imaging and Causal Pharmacological Inactivation in Macaques.

In primates, the presence of a face in a visual scene captures attention and rapidly directs the observer's gaze to the face, even when the face is not relevant to the task at hand. Here, we explored a neural circuit that might potentially play a causal role in this powerful behavior. In our previous research, two monkeys received microinfusions of muscimol, a GABAA-receptor agonist, or saline (as a control condition) in separate sessions into individual or pairs of four inferotemporal face patches (middle and anterior lateral and fundal), as identified by a preceding face localizer experiment. Then, using fMRI, we measured the impact of each inactivation condition on responses in the other face patches relative to the control condition. In this study, we used the same method and measured the impact of each inactivation condition on responses in the FEF and the lateral intraparietal area, two regions associated with attentional processing, while face and nonface object stimuli were viewed. Our results revealed potential relationships between inferotemporal face patches and these two attention-related regions: The inactivation of the middle lateral and anterior fundal face patches had a pronounced impact on FEF, whereas the inactivation of the middle and anterior lateral face patches might have a noticeable influence on lateral intraparietal area. Together, these initial exploratory findings document a circuit that potentially underlies the attentional capture of faces. Confirmation of the role of this circuit remains to be accomplished in the context of paradigm explicitly testing the attentional capture of faces.

Atypical reliance on monocular visual pathway for face and word recognition in developmental dyslexia.

Studies with individuals with developmental dyslexia (DD) have documented impaired perception of words and faces, both of which are domains of visual expertise for human adults. In this study, we examined a possible mechanism that might be associated with the impaired acquisition of visual expertise for words and faces in DD, namely, the atypical engagement of the monocular visual pathway. Participants with DD and typical readers (TR) judged whether a pair of sequentially presented unfamiliar faces or nonwords were the same or different, and the pair of stimuli were displayed in an eye-specific fashion using a stereoscope. Based on evidence of greater reliance on subcortical structures early in development, we predicted differences between the groups in the engagement of lower (monocular) versus higher (binocular) regions of the visual pathways. Whereas the TR group showed a monocular advantage for both stimulus types, the DD participants evinced a monocular advantage for faces and words that was much greater than that measured in the TRs. These findings indicate that the DD individuals have enhanced subcortical engagement and that this might arise from the failure to fine-tune cortical correlates mediating the discrimination of homogeneous exemplars in domains of expertise.

The Dorsal Visual Pathway Represents Object-Centered Spatial Relations for Object Recognition.

Although there is mounting evidence that input from the dorsal visual pathway is crucial for object processes in the ventral pathway, the specific functional contributions of dorsal cortex to these processes remain poorly understood. Here, we hypothesized that dorsal cortex computes the spatial relations among an object's parts, a process crucial for forming global shape percepts, and transmits this information to the ventral pathway to support object categorization. Using fMRI with human participants (females and males), we discovered regions in the intraparietal sulcus (IPS) that were selectively involved in computing object-centered part relations. These regions exhibited task-dependent functional and effective connectivity with ventral cortex, and were distinct from other dorsal regions, such as those representing allocentric relations, 3D shape, and tools. In a subsequent experiment, we found that the multivariate response of posterior (p)IPS, defined on the basis of part-relations, could be used to decode object category at levels comparable to ventral object regions. Moreover, mediation and multivariate effective connectivity analyses further suggested that IPS may account for representations of part relations in the ventral pathway. Together, our results highlight specific contributions of the dorsal visual pathway to object recognition. We suggest that dorsal cortex is a crucial source of input to the ventral pathway and may support the ability to categorize objects on the basis of global shape.SIGNIFICANCE STATEMENT Humans categorize novel objects rapidly and effortlessly. Such categorization is achieved by representing an object's global shape structure, that is, the relations among object parts. Yet, despite their importance, it is unclear how part relations are represented neurally. Here, we hypothesized that object-centered part relations may be computed by the dorsal visual pathway, which is typically implicated in visuospatial processing. Using fMRI, we identified regions selective for the part relations in dorsal cortex. We found that these regions can support object categorization, and even mediate representations of part relations in the ventral pathway, the region typically thought to support object categorization. Together, these findings shed light on the broader network of brain regions that support object categorization.

Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium.

Small average differences in the left-right asymmetry of cerebral cortical thickness have been reported in individuals with autism spectrum disorder (ASD) compared to typically developing controls, affecting widespread cortical regions. The possible impacts of these regional alterations in terms of structural network effects have not previously been characterized. Inter-regional morphological covariance analysis can capture network connectivity between different cortical areas at the macroscale level. Here, we used cortical thickness data from 1455 individuals with ASD and 1560 controls, across 43 independent datasets of the ENIGMA consortium's ASD Working Group, to assess hemispheric asymmetries of intra-individual structural covariance networks, using graph theory-based topological metrics. Compared with typical features of small-world architecture in controls, the ASD sample showed significantly altered average asymmetry of networks involving the fusiform, rostral middle frontal, and medial orbitofrontal cortex, involving higher randomization of the corresponding right-hemispheric networks in ASD. A network involving the superior frontal cortex showed decreased right-hemisphere randomization. Based on comparisons with meta-analyzed functional neuroimaging data, the altered connectivity asymmetry particularly affected networks that subserve executive functions, language-related and sensorimotor processes. These findings provide a network-level characterization of altered left-right brain asymmetry in ASD, based on a large combined sample. Altered asymmetrical brain development in ASD may be partly propagated among spatially distant regions through structural connectivity.

Developmental emergence of holistic processing in word recognition.

Holistic processing (HP) of faces refers to the obligatory, simultaneous processing of the parts and their relations, and it emerges over the course of development. HP is manifest in a decrement in the perception of inverted versus upright faces and a reduction in face processing ability when the relations between parts are perturbed. Here, adopting the HP framework for faces, we examined the developmental emergence of HP in another domain for which human adults have expertise, namely, visual word processing. Children, adolescents, and adults performed a lexical decision task and we used two established signatures of HP for faces: the advantage in perception of upright over inverted words and nonwords and the reduced sensitivity to increasing parts (word length). Relative to the other groups, children showed less of an advantage for upright versus inverted trials and lexical decision was more affected by increasing word length. Performance on these HP indices was strongly associated with age and with reading proficiency. Also, the emergence of HP for word perception was not simply a result of improved visual perception over the course of development as no group differences were observed on an object decision task. These results reveal the developmental emergence of HP for orthographic input, and reflect a further instance of experience-dependent tuning of visual perception. These results also add to existing findings on the commonalities of mechanisms of word and face recognition. RESEARCH HIGHLIGHTS: Children showed less of an advantage for upright versus inverted trials compared to adolescents and adults. Relative to the other groups, lexical decision in children was more affected by increasing word length. Performance on holistic processing (HP) indices was strongly associated with age and with reading proficiency. HP emergence for word perception was not due to improved visual perception over development as there were no group differences on an object decision task.

Exemplar learning reveals the representational origins of expert category perception.

Irrespective of whether one has substantial perceptual expertise for a class of stimuli, an observer invariably encounters novel exemplars from this class. To understand how novel exemplars are represented, we examined the extent to which previous experience with a category constrains the acquisition and nature of representation of subsequent exemplars from that category. Participants completed a perceptual training paradigm with either novel other-race faces (category of experience) or novel computer-generated objects (YUFOs) that included pairwise similarity ratings at the beginning, middle, and end of training, and a 20-d visual search training task on a subset of category exemplars. Analyses of pairwise similarity ratings revealed multiple dissociations between the representational spaces for those learning faces and those learning YUFOs. First, representational distance changes were more selective for faces than YUFOs; trained faces exhibited greater magnitude in representational distance change relative to untrained faces, whereas this trained-untrained distance change was much smaller for YUFOs. Second, there was a difference in where the representational distance changes were observed; for faces, representations that were closer together before training exhibited a greater distance change relative to those that were farther apart before training. For YUFOs, however, the distance changes occurred more uniformly across representational space. Last, there was a decrease in dimensionality of the representational space after training on YUFOs, but not after training on faces. Together, these findings demonstrate how previous category experience governs representational patterns of exemplar learning as well as the underlying dimensionality of the representational space.

Consortium neuroscience of attention deficit/hyperactivity disorder and autism spectrum disorder: The ENIGMA adventure.

Neuroimaging has been extensively used to study brain structure and function in individuals with attention deficit/hyperactivity disorder (ADHD) and autism spectrum disorder (ASD) over the past decades. Two of the main shortcomings of the neuroimaging literature of these disorders are the small sample sizes employed and the heterogeneity of methods used. In 2013 and 2014, the ENIGMA-ADHD and ENIGMA-ASD working groups were respectively, founded with a common goal to address these limitations. Here, we provide a narrative review of the thus far completed and still ongoing projects of these working groups. Due to an implicitly hierarchical psychiatric diagnostic classification system, the fields of ADHD and ASD have developed largely in isolation, despite the considerable overlap in the occurrence of the disorders. The collaboration between the ENIGMA-ADHD and -ASD working groups seeks to bring the neuroimaging efforts of the two disorders closer together. The outcomes of case-control studies of subcortical and cortical structures showed that subcortical volumes are similarly affected in ASD and ADHD, albeit with small effect sizes. Cortical analyses identified unique differences in each disorder, but also considerable overlap between the two, specifically in cortical thickness. Ongoing work is examining alternative research questions, such as brain laterality, prediction of case-control status, and anatomical heterogeneity. In brief, great strides have been made toward fulfilling the aims of the ENIGMA collaborations, while new ideas and follow-up analyses continue that include more imaging modalities (diffusion MRI and resting-state functional MRI), collaborations with other large databases, and samples with dual diagnoses.

How do the blind 'see'? The role of spontaneous brain activity in self-generated perception.

Spontaneous activity of the human brain has been well documented, but little is known about the functional role of this ubiquitous neural phenomenon. It has previously been hypothesized that spontaneous brain activity underlies unprompted (internally generated) behaviour. We tested whether spontaneous brain activity might underlie internally-generated vision by studying the cortical visual system of five blind/visually-impaired individuals who experience vivid visual hallucinations (Charles Bonnet syndrome). Neural populations in the visual system of these individuals are deprived of external input, which may lead to their hyper-sensitization to spontaneous activity fluctuations. To test whether these spontaneous fluctuations can subserve visual hallucinations, the functional MRI brain activity of participants with Charles Bonnet syndrome obtained while they reported their hallucinations (spontaneous internally-generated vision) was compared to the: (i) brain activity evoked by veridical vision (externally-triggered vision) in sighted controls who were presented with a visual simulation of the hallucinatory streams; and (ii) brain activity of non-hallucinating blind controls during visual imagery (cued internally-generated vision). All conditions showed activity spanning large portions of the visual system. However, only the hallucination condition in the Charles Bonnet syndrome participants demonstrated unique temporal dynamics, characterized by a slow build-up of neural activity prior to the reported onset of hallucinations. This build-up was most pronounced in early visual cortex and then decayed along the visual hierarchy. These results suggest that, in the absence of external visual input, a build-up of spontaneous fluctuations in early visual cortex may activate the visual hierarchy, thereby triggering the experience of vision.

Uncharacteristic Task-Evoked Pupillary Responses Implicate Atypical Locus Ceruleus Activity in Autism.

Autism spectrum disorder (ASD) is characterized partly by atypical attentional engagement, reflected in exaggerated and variable responses to sensory stimuli. Attentional engagement is known to be regulated by the locus ceruleus (LC). Moderate baseline LC activity globally dampens neural responsivity and is associated with adaptive deployment and narrowing of attention to task-relevant stimuli. In contrast, increased baseline LC activity enhances neural responsivity across cortex and widening of attention to environmental stimuli regardless of their task relevance. Given attentional atypicalities in ASD, this study is the first to evaluate whether, under different attentional task demands, individuals with ASD exhibit a different profile of LC activity compared with typically developing controls. Males and females with ASD and age- and gender-matched controls participated in a one-back letter detection test while task-evoked pupillary responses, an established correlate for LC activity, were recorded. Participants completed this task in two conditions, either in the absence or presence of distractor auditory tones. Compared with controls, individuals with ASD evinced atypical pupillary responses in the presence versus absence of distractors. Notably, this atypical pupillary profile was evident despite the fact that both groups exhibited equivalent task performance. Moreover, between-group differences in pupillary responses were observed specifically in response to task-relevant events, providing confirmation that the group differences most likely were specifically associated with distinctions in LC activity. These findings suggest that individuals with ASD show atypical modulation of LC activity with changes in attentional demands, offering a possible mechanistic and neurobiological account for attentional atypicalities in ASD.SIGNIFICANCE STATEMENT Individuals with autism spectrum disorder (ASD) exhibit atypical attentional behaviors, including altered sensory responses and atypical fixedness, but the neural mechanism underlying these behaviors remains elusive. One candidate mechanism is atypical locus ceruleus (LC) activity, as the LC plays a critical role in attentional modulation. Specifically, LC activity is involved in regulating the trade-off between environmental exploration and focused attention. This study shows that, under tightly controlled conditions, task-evoked pupil responses, an LC activity proxy, are lower in individuals with ASD than in controls, but only in the presence of task-irrelevant stimuli. This suggests that individuals with ASD evince atypical modulation of LC activity in accordance with changes in attentional demands, offering a mechanistic account for attentional atypicalities in ASD.

Changes in Cortical Coherence Supporting Complex Visual and Social Processing in Adolescence.

Despite our differences, there is much about the natural visual world that most observers perceive in common. Across adults, approximately 30% of the brain is activated in a consistent fashion while viewing naturalistic input. At what stage of development is this consistency of neural profile across individuals present? Here, we focused specifically on whether this mature profile is present in adolescence, a key developmental period that bridges childhood and adulthood, and in which new cognitive and social challenges are at play. We acquired fMRI data evoked by a movie shown twice to younger (9-14 years old) and older adolescents (15-19 years old) and to adults, and conducted three key analyses. First, we characterized the consistency of the neural response within individuals (across separate runs of the movie), then within individuals of the same age group, and, last, between age groups. The neural consistency within individuals was similar across age groups with reliable activation in largely overlapping but slightly different cortical regions. In contrast, somewhat differing regions exhibited higher within-age correlations in both groups of adolescents than in the adults. Last, across the whole cortex, we identified regions evincing different patterns of maturation across age. Together, these findings provide a fine-grained characterization of functional neural development in adolescence and uncover signatures of widespread change in cortical coherence that supports the emerging mature stereotypical responses to naturalistic stimuli. These results also offer a more nuanced account of development that obeys neither a rigid linear progression nor a large qualitative change over time.

Subcortical regions of the human visual system do not process faces holistically.

Face perception is considered to be evolutionarily adaptive and conserved across species. While subcortical visual brain areas are implicated in face perception based on existing evidence from phylogenetic and ontogenetic studies, whether these subcortical structures contribute to more complex visual computations such as the holistic processing (HP) of faces in humans is unknown. To address this issue, we used a well-established marker of HP, the composite face effect (CFE), with a group of adult human observers, and presented two sequential faces in a trial monocularly or interocularly using a Wheatstone stereoscope. HP refers to the finding that two identical top (or bottom) halves of a face are judged to be different when their task-irrelevant bottom (or top) halves belong to different faces. Because humans process faces holistically, they are unable to ignore the information from the irrelevant half of the composite face, and this is true to an even greater extent when the two halves of the faces are aligned compared with when they are misaligned ('Alignment effect'). The results revealed the HP effect and also uncovered the Alignment effect, a key marker of the CFE. The findings also indicated a monocular advantage, replicating the known subcortical contribution to face perception. There was, however, no statistically significant difference in the CFE when the images were presented in the monocular versus interocular conditions. These findings indicate that HP is not necessarily mediated by the subcortical visual pathway, and suggest that further investigation of cortical, rather than subcortical, structures might advance our understanding of HP and its role in face processing.

Perceptual Function and Category-Selective Neural Organization in Children with Resections of Visual Cortex.

The consequences of cortical resection, a treatment for humans with pharmaco-resistant epilepsy, provide a unique opportunity to advance our understanding of the nature and extent of cortical (re)organization. Despite the importance of visual processing in daily life, the neural and perceptual sequellae of occipitotemporal resections remain largely unexplored. Using psychophysical and fMRI investigations, we compared the neural and visuoperceptual profiles of 10 children or adolescents following unilateral cortical resections and their age- and gender-matched controls. Dramatically, with the exception of two individuals, both of whom had relatively greater cortical alterations, all patients showed normal perceptual performance on tasks of intermediate- and high-level vision, including face and object recognition. Consistently, again with the exception of the same two individuals, both univariate and multivariate fMRI analyses revealed normal selectivity and representational structure of category-selective regions. Furthermore, the spatial organization of category-selective regions obeyed the typical medial-to-lateral topographic organization albeit unilaterally in the structurally preserved hemisphere rather than bilaterally. These findings offer novel insights into the malleability of cortex in the pediatric population and suggest that, although experience may be necessary for the emergence of neural category-selectivity, this emergence is not necessarily contingent on the integrity of particular cortical structures.SIGNIFICANCE STATEMENT One approach to reduce seizure activity in patients with pharmaco-resistant epilepsy involves the resection of the epileptogenic focus. The impact of these resections on the perceptual behaviors and organization of visual cortex remain largely unexplored. Here, we characterized the visuoperceptual and neural profiles of ventral visual cortex in a relatively large sample of post-resection pediatric patients. Two major findings emerged. First, most patients exhibited preserved visuoperceptual performance across a wide-range of visual behaviors. Second, normal topography, magnitude, and representational structure of category-selective organization were uncovered in the spared hemisphere. These comprehensive imaging and behavioral investigations uncovered novel evidence concerning the neural representations and visual functions in children who have undergone cortical resection, and have implications for cortical plasticity more generally.

Effects of unilateral cortical resection of the visual cortex on bilateral human white matter.

Children with unilateral resections of ventral occipito-temporal cortex (VOTC) typically do not evince visual perceptual impairments, even when relatively large swathes of VOTC are resected. In search of possible explanations for this behavioral competence, we evaluated white matter microstructure and connectivity in eight pediatric epilepsy patients following unilateral cortical resection and 15 age-matched controls. To uncover both local and broader resection-induced effects, we analyzed tractography data using two complementary approaches. First, the microstructural properties were measured in the inferior longitudinal and the inferior fronto-occipital fasciculi, the major VOTC association tracts. Group differences were only evident in the ipsilesional, and not in the contralesional, hemisphere, and single-subject analyses revealed that these differences were limited to the site of the resection. Second, graph theory was used to characterize the connectivity of the contralesional occipito-temporal regions. There were no changes to the network properties in patients with left VOTC resections nor in patients with resections outside the VOTC, but altered network efficiency was observed in two cases with right VOTC resections. These results suggest that, in many, although perhaps not all, cases of unilateral VOTC resections in childhood, the white matter profile in the preserved contralesional hemisphere along with residual neural activity might be sufficient for normal visual perception.

Numerosity representation is encoded in human subcortex.

Certain numerical abilities appear to be relatively ubiquitous in the animal kingdom, including the ability to recognize and differentiate relative quantities. This skill is present in human adults and children, as well as in nonhuman primates and, perhaps surprisingly, is also demonstrated by lower species such as mosquitofish and spiders, despite the absence of cortical computation available to primates. This ubiquity of numerical competence suggests that representations that connect to numerical tasks are likely subserved by evolutionarily conserved regions of the nervous system. Here, we test the hypothesis that the evaluation of relative numerical quantities is subserved by lower-order brain structures in humans. Using a monocular/dichoptic paradigm, across four experiments, we show that the discrimination of displays, consisting of both large (5-80) and small (1-4) numbers of dots, is facilitated in the monocular, subcortical portions of the visual system. This is only the case, however, when observers evaluate larger ratios of 3:1 or 4:1, but not smaller ratios, closer to 1:1. This profile of competence matches closely the skill with which newborn infants and other species can discriminate numerical quantity. These findings suggest conservation of ontogenetically and phylogenetically lower-order systems in adults' numerical abilities. The involvement of subcortical structures in representing numerical quantities provokes a reconsideration of current theories of the neural basis of numerical cognition, inasmuch as it bolsters the cross-species continuity of the biological system for numerical abilities.

Spatiotemporal dynamics of similarity-based neural representations of facial identity.

Humans' remarkable ability to quickly and accurately discriminate among thousands of highly similar complex objects demands rapid and precise neural computations. To elucidate the process by which this is achieved, we used magnetoencephalography to measure spatiotemporal patterns of neural activity with high temporal resolution during visual discrimination among a large and carefully controlled set of faces. We also compared these neural data to lower level "image-based" and higher level "identity-based" model-based representations of our stimuli and to behavioral similarity judgments of our stimuli. Between ∼50 and 400 ms after stimulus onset, face-selective sources in right lateral occipital cortex and right fusiform gyrus and sources in a control region (left V1) yielded successful classification of facial identity. In all regions, early responses were more similar to the image-based representation than to the identity-based representation. In the face-selective regions only, responses were more similar to the identity-based representation at several time points after 200 ms. Behavioral responses were more similar to the identity-based representation than to the image-based representation, and their structure was predicted by responses in the face-selective regions. These results provide a temporally precise description of the transformation from low- to high-level representations of facial identity in human face-selective cortex and demonstrate that face-selective cortical regions represent multiple distinct types of information about face identity at different times over the first 500 ms after stimulus onset. These results have important implications for understanding the rapid emergence of fine-grained, high-level representations of object identity, a computation essential to human visual expertise.

Protracted Developmental Trajectory of Shape Processing along the Two Visual Pathways.

Studies of the emergence of shape representations in childhood have focused primarily on the ventral visual pathway. Importantly, however, there is increasing evidence that, in adults, the dorsal pathway also represents shape-based information. These dorsal representations follow a gradient with more posterior regions being more shape-sensitive than anterior regions and with representational similarity in some posterior regions that is equivalent to that observed in some ventral regions. To explore the emergence and nature of dorsal shape representations in development, we acquired both fMRI BOLD signals and behavioral data in children (aged 8-10 years) using a parametric image scrambling paradigm. Children exhibited adult-like large-scale organization of shape processing along both ventral and dorsal pathways. Also, as in adults, the activation profiles of children's posterior dorsal and ventral regions were correlated with recognition performance, reflecting a possible contribution of these signals to perception. There were age-related changes, however, with children being more affected by the distortion of shape information than adults, both behaviorally and neurally. These findings reveal that shape-processing mechanisms along both dorsal and ventral pathways are subject to a protracted developmental trajectory.

Temporal Dynamics of Shape Processing Differentiate Contributions of Dorsal and Ventral Visual Pathways.

Although shape perception is primarily considered a function of the ventral visual pathway, previous research has shown that both dorsal and ventral pathways represent shape information. Here, we examine whether the shape-selective electrophysiological signals observed in dorsal cortex are a product of the connectivity to ventral cortex or are independently computed. We conducted multiple EEG studies in which we manipulated the input parameters of the stimuli so as to bias processing to either the dorsal or ventral visual pathway. Participants viewed displays of common objects with shape information parametrically degraded across five levels. We measured shape sensitivity by regressing the amplitude of the evoked signal against the degree of stimulus scrambling. Experiment 1, which included grayscale versions of the stimuli, served as a benchmark establishing the temporal pattern of shape processing during typical object perception. These stimuli evoked broad and sustained patterns of shape sensitivity beginning as early as 50 msec after stimulus onset. In Experiments 2 and 3, we calibrated the stimuli such that visual information was delivered primarily through parvocellular inputs, which mainly project to the ventral pathway, or through koniocellular inputs, which mainly project to the dorsal pathway. In the second and third experiments, shape sensitivity was observed, but in distinct spatio-temporal configurations from each other and from that elicited by grayscale inputs. Of particular interest, in the koniocellular condition, shape selectivity emerged earlier than in the parvocellular condition. These findings support the conclusion of distinct dorsal pathway computations of object shape, independent from the ventral pathway.