The processes of recognizing objects and acting upon or with them have traditionally been attributed to computations associated with ventral and dorsal visual pathways, respectively. Accumulating evidence indicates that specific regions of the two pathways interact but the extent and strength of the whole-brain network connectivity remain to be evaluated. Here, in two experiments, we characterized the whole-brain network connections of object-selective seeds in each pathway using multiple analytic approaches with functional MRI data acquired while participants viewed objects. The results revealed substantial spatial overlap in connectivity in the networks generated from a dorsal and a ventral seed - with the greater similarity of these object networks within an individual than the similarity of each network separately across individuals. This overlap persisted for both tools and non-tools even after controlling for the shared variance between pathways. Notably, the dorsal pathway showed overall stronger and more widespread connectivity than the ventral pathway and was a stronger source of effective connectivity across the brain. Together, these findings reveal that dorsal and ventral pathways form highly overlapping and distributed networks in the service of object perception.
Seeing the world feels effortless, yet it is accomplished by two hemispheres that do not process visual information in the same way. Whether this involves distinct processing cascades, tight hemispheric coupling, or something in between has fundamental implications for understanding the emergence of coherent perception from divided processes. Images presented to the fovea project to both hemispheres, offering an opportunity to isolate intrinsic hemispheric differences in visual coding. Here, we used electroencephalography and neural decoding methods to investigate the dynamics of foveal visual processing in the left and right hemispheres. Human participants (N = 20; 15 females, 5 males) viewed images of objects, faces and words in rapid sequences while performing an orthogonal task. We found different trajectories of visual coding within the left and right hemispheres, and these differences were characterised by distinct featural biases in each hemisphere, with a particular left bias for rectilinearity and right bias for colour. Yet, despite encoding visual information differently, the left and right hemispheres appear to converge on a shared representation. The results provide new insights into hemispheric dynamics underlying visual perception and the complementary roles of the left and right hemispheres in processing visual information.
Characterization of the structural integrity of cortex in adults who have undergone resection for epilepsy treatment has revealed persistent or even accelerated cortical atrophy in some cases, but, in other cases, the converse is evident, and atrophy can decelerate or even be reversed. Whether this variability applies to a pediatric population, for whom postoperative plasticity may be greater than in adulthood, remains to be determined. Furthermore, understanding the morphometrics of this patient population is important, as cognitive gains have been associated with the anatomical status of the preserved cortex post-resection. Here, we used high-resolution structural T1 magnetic resonance imaging data to compare the (1) gross anatomy, (2) cortical thickness, volume, and surface area for 34 cortical regions, and (3) volume for nine subcortical regions of 32 pediatric post-surgical cases and 51 healthy controls. We only analyze the metrics from the preserved hemisphere. Relative to controls, patients with either a preserved right hemisphere (RH) or left hemisphere (LH) had significantly lower total white matter volume and larger lateral ventricle size, as well as a reduction of the volume of select subcortical structures. However, relative to controls, only patients with a preserved RH had significantly lower total gray matter volume and lower thickness, volume, and surface area in multiple cortical regions, primarily in the frontal and temporal cortex. The differences in the preserved RH cortex of LH resection patients may relate to transfer of language function from the affected LH. Our findings lay the foundation for future studies probing associations of the morphometric differences in pediatric epilepsy surgery patients with neuropsychological outcomes.
The ventral temporal cortex (VTC) of the human cerebrum is critically engaged in high-level vision. One intriguing aspect of this region is its functional lateralization, with neural responses to words being stronger in the left hemisphere, and neural responses to faces being stronger in the right hemisphere; such patterns can be summarized with a signed laterality index (LI), positive for leftward laterality. Converging evidence has suggested that word laterality emerges to couple efficiently with left-lateralized frontotemporal language regions, but evidence is more mixed regarding the sources of the right lateralization for face perception. Here, we use individual differences as a tool to test three theories of VTC organization arising from (1) local competition between words and faces driven by long-range coupling between words and language processes, (2) local competition between faces and other categories, and (3) long-range coupling with VTC and temporal areas exhibiting local competition between language and social processing. First, in an in-house functional MRI experiment, we did not obtain a negative correlation in the LIs of word and face selectivity relative to object responses, but did find a positive correlation when using selectivity relative to a fixation baseline, challenging ideas of local competition between words and faces driving rightward face lateralization. We next examined broader local LI interactions with faces using the large-scale Human Connectome Project (HCP) dataset. Face and tool LIs were significantly anti-correlated, while face and body LIs were positively correlated, consistent with the idea that generic local representational competition and cooperation may shape face lateralization. Last, we assessed the role of long-range coupling in the development of VTC lateralization. Within our in-house experiment, substantial positive correlation was evident between VTC text LI and that of several other nodes of a distributed text-processing circuit. In the HCP data, VTC face LI was both negatively correlated with language LI and positively correlated with social processing in different subregions of the posterior temporal lobe (PSL and STSp, respectively). In summary, we find no evidence of local face-word competition in VTC; instead, more generic local interactions shape multiple lateralities within VTC, including face laterality. Moreover, face laterality is also influenced by long-range coupling with social processing in the posterior temporal lobe, where social processing may become right lateralized due to local competition with language.
Characterization of the structural integrity of cortex in adults who have undergone resection for epilepsy treatment has, in some cases, revealed persistent or even accelerated cortical atrophy but, in others, the converse is evident, and atrophy decelerates or even reverses. Whether this variability applies to a pediatric population, for whom postoperative plasticity may be greater than in adulthood, remains to be determined. Furthermore, understanding the morphometrics of this patient population is important, as cognitive gains have been associated with the anatomical status of preserved cortex post-resection. Here, we used high-resolution structural T1 magnetic resonance imaging data to compare the (1) gross anatomy, (2) cortical thickness, volume, and surface area for 34 cortical regions, and (3) volume for nine subcortical regions of 32 pediatric post-surgical cases and 51 healthy controls. Patients with either a preserved right hemisphere (RH) or left hemisphere (LH) had lower total white matter volume and select subcortical structures' volumes, relative to controls; lateral ventricle size of both preserved RH and LH patients was also significantly larger than that of controls. However, relative to controls, only patients with a preserved RH had significantly lower total gray matter volume and lower thickness, volume, and surface area in multiple cortical regions, primarily in frontal and temporal cortex. The differences in preserved RH cortex of LH resection patients may relate to transfer of language function from the resected LH. Our findings lay the foundation for future studies probing associations of the morphometric differences in pediatric epilepsy surgery patients with neuropsychological outcomes.
This article reviews research that examines the topographic organization of the human brain, the role of development, breakdown and plasticity, and the constraints that give rise to the replicable organization across individuals and cultures. To address these questions, we evaluate the topographic arrangement of regions in ventral temporal cortex (VTC) that respond strongly to the viewing of faces and words, and demonstrate that both categories drive responses in both hemispheres albeit to a greater degree in the right hemisphere for faces and left hemisphere for words. We hypothesize that this weighted asymmetric topography emerges over the course of development, and we instantiate the hypothesis within a computational model and confirm predictions of this account with evidence from normal and impaired behavior and from neuroimaging. We also confront challenges to a particular component of this account, namely, the status of the local competition between word and face representations in VTC, and we go on to describe an expanded perspective with additional empirical data and a more complex computational framework, which highlights the generality of both local and long-range constraints on the emergence of within- and between-hemisphere topographic organization. Together, these findings offer a framework in which topographic organization emerges through an optimization process constrained by biological connectivity, the nature of the visual representations and development.
The neural circuitry engaged in supporting eye movements has been well characterized, but fundamental questions remain about the necessity and sufficiency of the individual hemispheric contributions. To gain a better understanding of the neural correlates of oculomotor control, we measured horizontal smooth pursuit tracking behavior in 14 patients following childhood hemispherectomy. Relative to developmentally typical age-matched controls, patients exhibited a bilateral and asymmetric pursuit deficit with reduced ipsilesional but elevated contralesional eye speeds, and asymmetric accompanying 'catch up' saccades. The atypical pursuit behavior could not be explained by a sensory deficit associated with their hemianopia, as patients adjusted their eye position to maintain visibility of the target. The pursuit deficit was also not accounted for by a general motor impairment as patients made faster catch-up saccades than controls, particularly in the ipsilesional direction. These results, all of which hold irrespective of whether the right or left hemisphere is resected, demonstrate that patients can compensate for reduced pursuit speeds by modulating their saccade characteristics. Overall, this study represents the most comprehensive characterization of smooth pursuit disturbances in hemispherectomy patients. Our results elucidate: 1) the competence of a single hemisphere for generating pursuit and compensatory behaviors; 2) the lack of a hemispheric bias supporting pursuit given large-scale cortical disruptions; and 3) that intact horizontal pursuit likely requires the interaction of brain circuitry across both hemispheres.
The brain consists of a multiplicity of networks with massively interacting nodes. Disruption of a node following brain damage can result in both short- and long-distance functional abnormalities, affecting even intact brain regions remote from the site of lesion (termed ‘diaschisis’). Diaschisis has been well described previously, and structural and functional connectivity have been related to clinical findings. However, the mechanistic and neurophysiological properties of this remote loss of function, its temporal and spectral dynamics, and its impact on the whole brain remain to be elucidated. In this study, we used high-density electroencephalography (EEG) to detect and characterize function- and frequency-dependent transcallosal diaschisis in a single-case of visual agnosia who has a perceptual deficit in object and face recognition following a focal lesion in the right posterior temporal cortex. Scalp EEG activity was evoked by images of intact and parametrically increased scrambled objects. SilenceMap, an algorithm developed for the location of reduced power (i.e., regions of silence), was used to estimate the slope of shape-selective EEG responses at levels of object scrambling, with structural and functional MRI serving as the ground truth for the lesion and diaschisis. The functional deficit, manifest as a significant reduction in the slope of EEG object shape sensitivity, was observed in the lesioned right ventral cortex and right dorsal cortex across most of the frequency bands (>4 Hz). This reduction in EEG slope was accompanied by contralesional diaschisis in the homotopic left ventral and left dorsal cortex but only in the Theta band (4−8Hz). This noninvasive approach both elucidates the neural correlates of diaschisis and confirms the viability of this approach in identifying neurological abnormality, perhaps offering a path toward precision medicine.
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. Notably, controls showed no significant RT cost differences between invalidly cued locations on cued versus uncued objects. By contrast, patients, irrespective of which hemisphere was resected, 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.
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 examine 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 compare the topography and neural representations of 17 category-selective regions in individuals with a VOTC resection, a 'control patient' with a resection outside VOTC, and typically developing matched controls. We demonstrate both adherence to and deviation from the standard topography, particularly with respect to the hemispheric lateralization of category-selective regions, and uncover 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.
The human brain continuously integrates information across its two hemispheres to construct a coherent representation of the perceptual world. Characterizing how visual information is represented in each hemisphere over time is crucial for understanding how hemispheric transfer contributes to perception. Here, we investigated information processing within each hemisphere over time and the degree to which it is distinct or duplicated across hemispheres. We presented participants with object images lateralized to the left or right visual fields while measuring their brain activity with electroencephalography. Stimulus coding was more robust and emerged earlier in the contralateral than the ipsilateral hemisphere. Presentation of two stimuli, one to each hemifield, reduced the fidelity of representations in both hemispheres relative to one stimulus alone, signifying hemispheric interference. Last, we found that processing within the contralateral, but not ipsilateral, hemisphere was biased to image-related over concept-related information. Together, these results suggest that hemispheric transfer operates to filter irrelevant information and efficiently prioritize processing of meaning.
Functional specialization within high-level vision is reflected in the topographic organization of the ventral temporal cortex (VTC). The presence and consistent locations of small areas responding selectively to particular visual categories – such as faces and scenes – has led to proposals of innate domain-specific modules. However, such proposals do not easily explain other aspects of an apparently multi-scale topographic organization of high-level visual features in VTC. Computational models have recently accounted for the presence of domain-selective areas and other facets of topographic organization from a basic optimization process with local topographic pressures, such as locally constrained connectivity, but fail to account for the consistent location of category-selectivity. In the current work, we extend a recent computational model to demonstrate how this consistency may emerge from wiring constraints external to VTC, focusing on the role of retinotopically organized early visual representations. After training several random initializations of the model, we find consistent global topographic organization, with face- and scene-selectivity emerging on opposite ends of a medial-lateral gradient corresponding to eccentricity bias, similar to human VTC. As in human VTC, the eccentricity-biased topography persists across viewing sizes under sufficiently broad viewing bias distributions, suggesting that it is a learned bias for efficiently organizing representations proximal to the most useful inputs, rather than merely an explicit retinotopic code. Abolishing the retinotopic constraint abolishes topographic consistency, but not topographic organization. Our work suggests that the organization of high-level visual cortex may emerge from domain-relevant interactions between viewing biases and task demands with an innate retinotopic scaffold. More generally, we suggest that both local and global connectivity constraints interact with representation learning to produce mature cortical organization: local constraints pressure the system towards smooth organization, whereas long-range constraints encourage a consistent global layout.
Single case studies have long been used to provide insights into the mechanisms underlying normal cognition, including in the domains of memory, language and visuoperceptual function, and standardized testing has been a steadfast companion in such investigations. Experimental approaches designed to address specific hypotheses have also been conducted and analytic methods have been developed for the comparison of single subject data to a control group. However, a seismic shift has occurred in the last decade or two in which neuroimaging, primarily magnetic resonance imaging, has been added to the experimental toolbox. The question addressed in this article is whether, with these newer methodologies offering novel and previously unattainable evidence, single case studies have become obsolete. Here, in a single patient with integrative visual agnosia, tested repeatedly over three decades, behavioral, neuroimaging and joint behavioral-neuroimaging studies are described and their yield evaluated. Behavioral investigations have served to characterize the perceptual deficit well, and structural and functional neuroimaging data have furthered our understanding of the distributed circuit engaged in object recognition. However, imaging studies executed in concert with a behavioral task have offered more direct causal evidence, providing a more complete understanding of brain-behavior correspondences that goes beyond the sum of the parts. The conclusion reached is that the contribution of causal evidence from single cases remains a powerful methodology in advancing our knowledge of the neural basis of cognition.
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 γ-aminobutyric acid type 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 an initial 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 had a noticeable influence on LIP. 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 a paradigm that explicitly tests the attentional capture of faces.
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.
Although the Visual Word Form Area (VWFA) in left temporal cortex is considered the pre-eminent region in visual word processing, other regions are also implicated. We examined the entire text-selective circuit, using functional MRI. Ten regions of interest (ROIs) per hemisphere were defined, which, based on clustering, grouped into early vision, high-level vision, and language clusters. We analyzed the responses of the ROIs and clusters to words, inverted words, and consonant strings using univariate, multivariate, and functional connectivity measures. Bilateral modulation by stimulus condition was evident, with a stronger effect in left hemisphere regions. Last, using graph theory, we observed that the VWFA was equivalently connected with early visual and language clusters in both hemispheres, reflecting its role as a mediator in the circuit. Although the individual ROIs and clusters bilaterally were flexibly altered by the nature of the input, stability held at the level of global circuit connectivity, reflecting the complex hierarchical distributed system serving visual text perception.