Observers deploy covert attention as a means of winnowing the complexity of visual scenes into manageable input that can be processed efficiently. The well-established 'two rectangle paradigm' has been widely used to characterize space- and object-based attention, associated with highlighting a particular spatial position or a particular object, respectively (Egly et al., 1994). Neuroimaging and neuropsychological studies have ascribed space-based attention predominantly to the fronto-parietal network in the right hemisphere (RH; e.g., Schotten et al., 2011) and object-based attention primarily to the left hemisphere (LH; e.g., Orlandi & Proverbio, 2019). Here, we address whether this hemispheric asymmetry is a fixed property of the RH versus LH or is amenable to functional reorganization in individuals who have only a single hemisphere. 23 participants with childhood hemispherectomy (9 with preserved LH and 14 with preserved RH) for the management of drug-resistant epilepsy, completed a modified, age-appropriate two-rectangle paradigm ("Help Doug the dog figure out the color of the missing ball"), comprised of 70% valid trials (cue and target in same location), 10% invalid space (cue and target at same end of two different rectangles), 10% invalid object (cue and target at different ends of the same rectangle) and 10% neutral trials (four rectangle ends cued, target position random). Both patient groups performed significantly better for the valid than other conditions on both accuracy and reaction time measures, which did not differ from each other. Interestingly, there was no main effect of patient group (side of resection). These surprising results indicate that either hemisphere can mediate both types of attention without hemisphere-specific advantages after loss of an entire hemisphere, perhaps reflecting plasticity and functional reorganization in childhood.
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.
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.
Smooth pursuit eye movements are crucial for tracking moving visual stimuli. This capacity is subserved by a bilateral network of brain regions including the frontal eye fields, basal ganglia, and occipitotemporal cortex (Sharpe, 2008, Lencer et al., 2008). Previous studies have demonstrated deficits in which adults with unilateral frontal or posterior lesions, or hemispherectomy execute saccades rather than smooth pursuit ipsilesionally (Morrow et al., 1995, Thurston et al., 1988, Troost et al., 1972). It is not known to what extent the smooth pursuit system is affected in those with childhood hemispherectomy for the treatment of drug-resistant epilepsy. We recorded eye movements using an EyeLink 1000 Plus during sinusoidal smooth pursuit in individuals with childhood hemispherectomy (n = 14, 10 left [LH] and 4 right [RH] hemispherectomies, age at surgery: < 1 month-8 years, age at test: 12-32 years). Participants tracked a target moving in a horizontal sinusoidal pattern (frequency = 0.3 Hz, amplitude = 10 degrees) for 4-12, 10 second trials. Qualitative visual analysis of sinusoidal trace plots shows that the participants generally followed the target, but had large variability in smooth pursuit, with many exhibiting frequent saccades, blinks, or other positional deviance from target position. To investigate possible asymmetries in this atypical pattern, we compared pursuit movements in the ipsilesional and contralesional direction for each participant. Every participant showed statistically significant differences between ipsilesional and contralesional movement variance (p < 0.05). To test whether these asymmetries can be explained by saccadic interruption of smooth pursuit, we computed the number of saccades during ipsilesional and contralesional movement from smoothed eye velocity traces. All 10 LH and one RH participant exhibited more ipsilesional than contralesional saccades. Surprisingly, the remaining RH participants did not show this atypical pattern. Overall, our results elucidate smooth pursuit asymmetries in individuals with childhood hemispherectomy.
Abstract Humans can label and categorize objects in a visual scene with high accuracy and speed—a capacity well-characterized with neuroimaging 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 in the brain, we created a novel stimulus set to isolate motion-defined signals from other sources of information. We extracted movement information from videos of 6 object categories and applied the motion to random dot patterns. Using these stimuli, we investigated whether fMRI responses elicited by motion cues could be decoded at the object category level in functionally defined regions of occipitotemporal and parietal cortex. Participants performed a one-back repetition detection task as they viewed motion-defined stimuli or static images from the original videos. Linear classifiers could decode object category for both stimulus formats in all higher order regions of interest. More posterior occipitotemporal and ventral regions showed higher accuracy in the static condition and more anterior occipitotemporal and dorsal regions showed higher accuracy in the dynamic condition. Significantly above chance classification accuracies were also observed in all regions when training and testing the SVM classifier across stimulus formats. These results demonstrate that motion-defined cues can elicit widespread robust category responses on par with those elicited by luminance cues in regions of object-selective visual cortex. The informational content of these responses overlapped with, but also demonstrated interesting distinctions from, those elicited by static cues. Significance Statement Much research on visual object recognition has focused on recognizing objects in static images. However, motion cues are 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 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.
Abstract The neural processes underlying attentional processing are typically lateralized in adults, with spatial attention associated with the right hemisphere (RH) and object-based attention with the left hemisphere (LH). Using a modified two-rectangle attention paradigm, we compared the lateralization profiles of individuals with childhood hemispherectomy (either LH or RH) and age-matched, typically developing controls. Although patients exhibited slower reaction times (RTs) compared to controls, both groups benefited from valid attentional cueing. However, patients experienced significantly higher costs for invalid trials—reflected by larger RT differences between validly and invalidly cued targets. This was true for invalid trials on both cued and uncued objects, probes of object- and space-based attentional processes, respectively. Notably, controls showed no significant RT cost differences between invalidly cued locations on cued versus uncued objects. By contrast, patients exhibited greater RT costs for targets on uncued versus cued objects, suggesting greater difficulty shifting attention across objects. We explore potential explanations for this group difference and the lack of difference between patients with LH or RH resection. These findings enhance our understanding of spatial and object-based attention in typical development and reveal how significant neural injury affects the development of attentional systems in the LH and RH.
Abstract The topographic organization of category-selective responses in human ventral occipitotemporal cortex (VOTC) and its relationship to regions subserving language functions is remarkably uniform across individuals. This arrangement is thought to result from the clustering of neurons responding to similar inputs, constrained by intrinsic architecture and tuned by experience. We examined the malleability of this organization in individuals with unilateral resection of VOTC during childhood for the management of drug-resistant epilepsy. In cross-sectional and longitudinal functional imaging studies, we compared the topography and neural representations of 17 category-selective regions in individuals with a VOTC resection, a ‘control patient’ with resection outside VOTC, and typically developing matched controls. We demonstrated both adherence to and deviation from the standard topography and uncovered fine-grained competitive dynamics between word- and face-selectivity over time in the single, preserved VOTC. The findings elucidate the nature and extent of cortical plasticity and highlight the potential for remodeling of extrastriate architecture and function. Teaser After pediatric cortical resection, deviations from the constraints of standard topography in visual cortex reflect plasticity.
'/%3e%3cuse xlink:href='%23a' transform='rotate(144 450 300)'/%3e%3cuse xlink:href='%23a' transform='rotate(216 450 300)'/%3e%3cuse xlink:href='%23a' transform='rotate(288 450 300)'/%3e%3c/svg%3e)