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.

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.

Disentangling Object Category Representations Driven by Dynamic and Static Visual Input.

Humans can label and categorize objects in a visual scene with high accuracy and speed, a capacity well characterized with studies using static images. However, motion is another cue that could be used by the visual system to classify objects. To determine how motion-defined object category information is processed by the brain in the absence of luminance-defined form information, we created a novel stimulus set of "object kinematograms" to isolate motion-defined signals from other sources of visual information. Object kinematograms were generated by extracting motion information from videos of 6 object categories and applying the motion to limited-lifetime random dot patterns. Using functional magnetic resonance imaging (fMRI) (n = 15, 40% women), we investigated whether category information from the object kinematograms could be decoded within the occipitotemporal and parietal cortex and evaluated whether the information overlapped with category responses to static images from the original videos. We decoded object category for both stimulus formats in all higher-order regions of interest (ROIs). More posterior occipitotemporal and ventral regions showed higher accuracy in the static condition, while more anterior occipitotemporal and dorsal regions showed higher accuracy in the dynamic condition. Further, decoding across the two stimulus formats was possible in all regions. These results demonstrate that motion cues can elicit widespread and robust category responses on par with those elicited by static luminance cues, even in ventral regions of visual cortex that have traditionally been associated with primarily image-defined form processing.SIGNIFICANCE STATEMENT Much research on visual object recognition has focused on recognizing objects in static images. However, motion is a rich source of information that humans might also use to categorize objects. Here, we present the first study to compare neural representations of several animate and inanimate objects when category information is presented in two formats: static cues or isolated dynamic motion cues. Our study shows that, while higher-order brain regions differentially process object categories depending on format, they also contain robust, abstract category representations that generalize across format. These results expand our previous understanding of motion-derived animate and inanimate object category processing and provide useful tools for future research on object category processing driven by multiple sources of visual information.

Curvilinear features are important for animate/inanimate categorization in macaques.

The current experiment investigated the extent to which perceptual categorization of animacy (i.e., the ability to discriminate animate and inanimate objects) is facilitated by image-based features that distinguish the two object categories. We show that, with nominal training, naïve macaques could classify a trial-unique set of 1000 novel images with high accuracy. To test whether image-based features that naturally differ between animate and inanimate objects, such as curvilinear and rectilinear information, contribute to the monkeys' accuracy, we created synthetic images using an algorithm that distorted the global shape of the original animate/inanimate images while maintaining their intermediate features (Portilla & Simoncelli, 2000). Performance on the synthesized images was significantly above chance and was predicted by the amount of curvilinear information in the images. Our results demonstrate that, without training, macaques can use an intermediate image feature, curvilinearity, to facilitate their categorization of animate and inanimate objects.

Curvature processing in human visual cortical areas.

Curvature is one of many visual features shown to be important for visual perception. We recently showed that curvilinear features provide sufficient information for categorizing animate vs. inanimate objects, while rectilinear features do not (Zachariou et al., 2018). Results from our fMRI study in rhesus monkeys (Yue et al., 2014) have shed light on some of the neural substrates underlying curvature processing by revealing a network of visual cortical patches with a curvature response preference. However, it is unknown whether a similar network exists in human visual cortex. Thus, the current study was designed to investigate cortical areas with a preference for curvature in the human brain using fMRI at 7T. Consistent with our monkey fMRI results, we found a network of curvature preferring cortical patches-some of which overlapped well-known face-selective areas. Moreover, principal component analysis (PCA) using all visually-responsive voxels indicated that curvilinear features of visual stimuli were associated with specific retinotopic regions in visual cortex. Regions associated with positive curvilinear PC values encompassed the central visual field representation of early visual areas and the lateral surface of temporal cortex, while those associated with negative curvilinear PC values encompassed the peripheral visual field representation of early visual areas and the medial surface of temporal cortex. Thus, we found that broad areas of curvature preference, which encompassed face-selective areas, were bound by central visual field representations. Our results support the hypothesis that curvilinearity preference interacts with central-peripheral processing biases as primary features underlying the organization of temporal cortex topography in the adult human brain.

Functional Resilience of the Neural Visual Recognition System Post-Pediatric Occipitotemporal Resection.

In the typically developing (TD) brain, neural representations for visual stimulus categories (e.g., faces, objects, and words) emerge in bilateral occipitotemporal cortex (OTC), albeit with weighted asymmetry; in parallel, recognition behavior continues to be refined. A fundamental question is whether two hemispheres are necessary or redundant for the emergence of neural representations and recognition behavior typically distributed across both hemispheres. The rare population of patients undergoing unilateral OTC resection in childhood offers a unique opportunity to evaluate whether neural computations for visual stimulus individuation suffice for recognition with only a single developing OTC. Here, using functional magnetic resonance imaging, we mapped category selectivity (CS) and neural representations for individual stimulus exemplars using repetition suppression (RS) in the non-resected hemisphere of pediatric OTC resection patients (n = 9) and control patients with resection outside of OTC (n = 12), as well as in both hemispheres of TD controls (n = 21). There were no univariate group differences in the magnitude of CS or RS or any multivariate differences (per representational similarity analysis) in neural activation to faces, objects, or words across groups. Notwithstanding their comparable neural profiles, accuracy of OTC resection patients on face and object recognition, but not word recognition, was statistically inferior to that of controls. The comparable neural signature of the OTC resection patients' preserved hemisphere and the other two groups highlights the resilience of the system following damage to the contralateral homologue. Critically, however, a single OTC does not suffice for normal behavior, and, thereby, implicates the necessity for two hemispheres.

Holistic processing and face expertise after pediatric resection of occipitotemporal cortex.

The nature and extent of hemispheric lateralization and its potential for reorganization continues to be debated, although there is general agreement that there is a right hemisphere (RH) advantage for face processing in human adults. Here, we examined face processing and its lateralization in individuals with a single preserved occipitotemporal cortex (OTC), either in the RH or left hemisphere (LH), following early childhood resection for the management of drug-resistant epilepsy. The matched controls and those with a lesion outside of OTC evinced the standard superiority in processing upright over inverted faces and the reverse sensitivity to a nonface category (bicycles). In contrast, the LH and the RH patient groups were significantly less accurate than the controls and showed mild orientation sensitivities at best (and not always in the predicted directions). For the two patient groups, the accuracies of face and bicycle processing did not differ from each other and were not obviously related to performance on intermediate level global form tasks with, again, poorer thresholds for both patient groups than controls and no difference between the patient groups. These findings shed light on the complexity of hemispheric lateralization and face and nonface object processing in individuals following surgical resection of OTC. Overall, this study highlights the unique dynamics and potential for plasticity in those with childhood cortical resection.

Differential functional reorganization of ventral and dorsal visual pathways following childhood hemispherectomy.

Hemispherectomy is a surgical procedure in which an entire hemisphere of a patient's brain is resected or functionally disconnected to manage seizures in individuals with drug-resistant epilepsy. Despite the extensive loss of input from both ventral and dorsal visual pathways of one hemisphere, pediatric patients who have undergone hemispherectomy show a remarkably high degree of perceptual function across many domains. In the current study, we sought to understand the extent to which functions of the ventral and dorsal visual pathways reorganize to the contralateral hemisphere following childhood hemispherectomy. To this end, we collected fMRI data from an equal number of left and right hemispherectomy patients who completed tasks that typically elicit lateralized responses from the ventral or the dorsal pathway, namely, word (left ventral), face (right ventral), tool (left dorsal), and global form (right dorsal) perception. Overall, there was greater evidence of functional reorganization in the ventral pathway than in the dorsal pathway. Importantly, because ventral and dorsal reorganization was tested in the very same patients, these results cannot be explained by idiosyncratic factors such as disease etiology, age at the time of surgery, or age at testing. These findings suggest that because the dorsal pathway may mature earlier, it may have a shorter developmental window of plasticity than the ventral pathway and, hence, be less malleable.

Differential functional reorganization of ventral and dorsal visual pathways following childhood hemispherectomy.

Hemispherectomy is a surgical procedure in which an entire hemisphere of a patient's brain is resected or functionally disconnected to manage seizures in individuals with drug-resistant epilepsy. Despite the extensive loss of both ventral and dorsal visual pathways in one hemisphere, pediatric patients who have undergone hemispherectomy show a remarkably high degree of perceptual function across many domains. In the current study, we sought to understand the extent to which functions of the ventral and dorsal visual pathways reorganize to the contralateral hemisphere following childhood hemispherectomy. To this end, we collected fMRI data from an equal number of left and right hemispherectomy patients who completed tasks that typically elicit lateralized responses from the ventral or the dorsal pathway, namely, word (left ventral), face (right ventral), tool (left dorsal), and global form (right dorsal) perception. Overall, there was greater evidence of functional reorganization in the ventral pathway than in the dorsal pathway. Importantly, because ventral and dorsal reorganization was tested within the very same patients, these results cannot be explained by idiosyncratic factors such as disease etiology, age at the time of surgery, or age at testing. These findings suggest that because the dorsal pathway may mature earlier, it may have a shorter developmental window of plasticity than the ventral pathway and, hence, be less malleable after perturbation.