Microstructural proliferation in human cortex is coupled with the development of face processing
2017; 355 (6320): 68-?
How does cortical tissue change as brain function and behavior improve from childhood to adulthood? By combining quantitative and functional magnetic resonance imaging in children and adults, we find differential development of high-level visual areas that are involved in face and place recognition. Development of face-selective regions, but not place-selective regions, is dominated by microstructural proliferation. This tissue development is correlated with specific increases in functional selectivity to faces, as well as improvements in face recognition, and ultimately leads to differentiated tissue properties between face- and place-selective regions in adulthood, which we validate with postmortem cytoarchitectonic measurements. These data suggest a new model by which emergent brain function and behavior result from cortical tissue proliferation rather than from pruning exclusively.
View details for DOI 10.1126/science.aag0311
View details for Web of Science ID 000391739900044
View details for PubMedID 28059764
View details for PubMedCentralID PMC5373008
- The Cytoarchitecture of Domain-specific Regions in Human High-level Visual Cortex CEREBRAL CORTEX 2017; 27 (1): 146-161
The Face-Processing Network Is Resilient to Focal Resection of Human Visual Cortex.
journal of neuroscience
2016; 36 (32): 8425-8440
Human face perception requires a network of brain regions distributed throughout the occipital and temporal lobes with a right hemisphere advantage. Present theories consider this network as either a processing hierarchy beginning with the inferior occipital gyrus (occipital face area; IOG-faces/OFA) or a multiple-route network with nonhierarchical components. The former predicts that removing IOG-faces/OFA will detrimentally affect downstream stages, whereas the latter does not. We tested this prediction in a human patient (Patient S.P.) requiring removal of the right inferior occipital cortex, including IOG-faces/OFA. We acquired multiple fMRI measurements in Patient S.P. before and after a preplanned surgery and multiple measurements in typical controls, enabling both within-subject/across-session comparisons (Patient S.P. before resection vs Patient S.P. after resection) and between-subject/across-session comparisons (Patient S.P. vs controls). We found that the spatial topology and selectivity of downstream ipsilateral face-selective regions were stable 1 and 8 month(s) after surgery. Additionally, the reliability of distributed patterns of face selectivity in Patient S.P. before versus after resection was not different from across-session reliability in controls. Nevertheless, postoperatively, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1 of the resected hemisphere. Diffusion weighted imaging in Patient S.P. and controls identifies white matter tracts connecting retinotopic areas to downstream face-selective regions, which may contribute to the stable and plastic features of the face network in Patient S.P. after surgery. Together, our results support a multiple-route network of face processing with nonhierarchical components and shed light on stable and plastic features of high-level visual cortex following focal brain damage.Brain networks consist of interconnected functional regions commonly organized in processing hierarchies. Prevailing theories predict that damage to the input of the hierarchy will detrimentally affect later stages. We tested this prediction with multiple brain measurements in a rare human patient requiring surgical removal of the putative input to a network processing faces. Surprisingly, the spatial topology and selectivity of downstream face-selective regions are stable after surgery. Nevertheless, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1. White matter connections from outside the face network may support these stable and plastic features. As processing hierarchies are ubiquitous in biological and nonbiological systems, our results have pervasive implications for understanding the construction of resilient networks.
View details for DOI 10.1523/JNEUROSCI.4509-15.2016
View details for PubMedID 27511014
View details for PubMedCentralID PMC4978802
The anatomical and functional specialization of the fusiform gyrus.
2016; 83: 48-62
The fusiform gyrus (FG) is commonly included in anatomical atlases and is considered a key structure for functionally-specialized computations of high-level vision such as face perception, object recognition, and reading. However, it is not widely known that the FG has a contentious history. In this review, we first provide a historical analysis of the discovery of the FG and why certain features, such as the mid-fusiform sulcus, were discovered and then forgotten. We then discuss how observer-independent methods for identifying cytoarchitectonical boundaries of the cortex revolutionized our understanding of cytoarchitecture and the correspondence between those boundaries and cortical folding patterns of the FG. We further explain that the co-occurrence between cortical folding patterns and cytoarchitectonical boundaries are more common than classically thought and also, are functionally meaningful especially on the FG and probably in high-level visual cortex more generally. We conclude by proposing a series of alternatives for how the anatomical organization of the FG can accommodate seemingly different theoretical aspects of functional processing, such as domain specificity and perceptual expertise.
View details for DOI 10.1016/j.neuropsychologia.2015.06.033
View details for PubMedID 26119921
- The posterior arcuate fasciculus and the vertical occipital fasciculus. Cortex; a journal devoted to the study of the nervous system and behavior 2016
Two New Cytoarchitectonic Areas on the Human Mid-Fusiform Gyrus.
Areas of the fusiform gyrus (FG) within human ventral temporal cortex (VTC) process high-level visual information associated with faces, limbs, words, and places. Since classical cytoarchitectonic maps do not adequately reflect the functional and structural heterogeneity of the VTC, we studied the cytoarchitectonic segregation in a region, which is rostral to the recently identified cytoarchitectonic areas FG1 and FG2. Using an observer-independent and statistically testable parcellation method, we identify 2 new areas, FG3 and FG4, in 10 human postmortem brains on the mid-FG. The mid-fusiform sulcus reliably identifies the cytoarchitectonic transition between FG3 and FG4. We registered these cytoarchitectonic areas to the common reference space of the single-subject Montreal Neurological Institute (MNI) template and generated probability maps, which reflect the intersubject variability of both areas. Future studies can relate in vivo neuroimaging data with these microscopically defined cortical areas to functional parcellations. We discuss these results in the context of both large-scale functional maps and fine-scale functional clusters that have been identified within the human VTC. We propose that our observer-independent cytoarchitectonic parcellation of the FG better explains the functional heterogeneity of the FG compared with the homogeneity of classic cytoarchitectonic maps.
View details for PubMedID 26464475
The evolution of face processing networks.
Trends in cognitive sciences
2015; 19 (5): 240-241
Recent studies in marmosets, macaques, and humans have begun to show commonalities and differences in the evolution of face processing networks. Despite differences in brain size and gyrification across species, myelination and motion may be key anatomical and functional features contributing to the surprising similarity of face networks across species.
View details for DOI 10.1016/j.tics.2015.03.010
View details for PubMedID 25840651
The vertical occipital fasciculus: A century of controversy resolved by in vivo measurements
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2014; 111 (48): E5214-E5223
The vertical occipital fasciculus (VOF) is the only major fiber bundle connecting dorsolateral and ventrolateral visual cortex. Only a handful of studies have examined the anatomy of the VOF or its role in cognition in the living human brain. Here, we trace the contentious history of the VOF, beginning with its original discovery in monkey by Wernicke (1881) and in human by Obersteiner (1888), to its disappearance from the literature, and recent reemergence a century later. We introduce an algorithm to identify the VOF in vivo using diffusion-weighted imaging and tractography, and show that the VOF can be found in every hemisphere (n = 74). Quantitative T1 measurements demonstrate that tissue properties, such as myelination, in the VOF differ from neighboring white-matter tracts. The terminations of the VOF are in consistent positions relative to cortical folding patterns in the dorsal and ventral visual streams. Recent findings demonstrate that these same anatomical locations also mark cytoarchitectonic and functional transitions in dorsal and ventral visual cortex. We conclude that the VOF is likely to serve a unique role in the communication of signals between regions on the ventral surface that are important for the perception of visual categories (e.g., words, faces, bodies, etc.) and regions on the dorsal surface involved in the control of eye movements, attention, and motion perception.
View details for DOI 10.1073/pnas.1418503111
View details for Web of Science ID 000345920800011
View details for PubMedID 25404310
The functional architecture of the ventral temporal cortex and its role in categorization.
Nature reviews. Neuroscience
2014; 15 (8): 536-548
Visual categorization is thought to occur in the human ventral temporal cortex (VTC), but how this categorization is achieved is still largely unknown. In this Review, we consider the computations and representations that are necessary for categorization and examine how the microanatomical and macroanatomical layout of the VTC might optimize them to achieve rapid and flexible visual categorization. We propose that efficient categorization is achieved by organizing representations in a nested spatial hierarchy in the VTC. This spatial hierarchy serves as a neural infrastructure for the representational hierarchy of visual information in the VTC and thereby enables flexible access to category information at several levels of abstraction.
View details for DOI 10.1038/nrn3747
View details for PubMedID 24962370
The mid-fusiform sulcus: A landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex
2014; 84: 453-465
Human ventral temporal cortex (VTC) plays a pivotal role in high-level vision. An under-studied macroanatomical feature of VTC is the mid-fusiform sulcus (MFS), a shallow longitudinal sulcus separating the lateral and medial fusiform gyrus (FG). Here, we quantified the morphological features of the MFS in 69 subjects (ages 7-40), and investigated its relationship to both cytoarchitectonic and functional divisions of VTC with four main findings. First, despite being a minor sulcus, we found that the MFS is a stable macroanatomical structure present in all 138 hemispheres with morphological characteristics developed by age 7. Second, the MFS is the locus of a lateral-medial cytoarchitectonic transition within the posterior FG serving as the boundary between cytoarchitectonic regions FG1 and FG2. Third, the MFS predicts a lateral-medial functional transition in eccentricity bias representations in children, adolescents, and adults. Fourth, the anterior tip of the MFS predicts the location of a face-selective region, mFus-faces/FFA-2. These findings are the first to illustrate that a macroanatomical landmark identifies both cytoarchitectonic and functional divisions of high-level sensory cortex in humans and have important implications for understanding functional and structural organization in the human brain.
View details for DOI 10.1016/j.neuroimage.2013.08.068
View details for Web of Science ID 000328868600042
View details for PubMedID 24021838
History: Two brains and a forgotten theory.
2014; 509 (7498): 33
View details for DOI 10.1038/509033e
The improbable simplicity of the fusiform face area
TRENDS IN COGNITIVE SCIENCES
2012; 16 (5): 251-254
The fusiform face area (FFA) is described as an easily identifiable module on the fusiform gyrus. However, the organization of face-selective regions in ventral temporal cortex (VTC) is more complex than this prevailing view. We highlight methodological factors contributing to these complexities and the extensive variability in how the FFA is identified. We suggest a series of constraints to aid researchers when defining any functionally specialized region with a pleasing realization: anatomy matters.
View details for DOI 10.1016/j.tics.2012.03.003
View details for Web of Science ID 000304026200001
View details for PubMedID 22481071
Not one extrastriate body area: Using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex
2011; 56 (4): 2183-2199
The prevailing view of human lateral occipitotemporal cortex (LOTC) organization suggests a single area selective for images of the human body (extrastriate body area, EBA) that highly overlaps with the human motion-selective complex (hMT+). Using functional magnetic resonance imaging with higher resolution (1.5mm voxels) than past studies (3-4mm voxels), we examined the fine-scale spatial organization of these activations relative to each other, as well as to visual field maps in LOTC. Rather than one contiguous EBA highly overlapping hMT+, results indicate three limb-selective activations organized in a crescent surrounding hMT+: (1) an activation posterior to hMT+ on the lateral occipital sulcus/middle occipital gyrus (LOS/MOG) overlapping the lower vertical meridian shared between visual field maps LO-2 and TO-1, (2) an activation anterior to hMT+ on the middle temporal gyrus (MTG) consistently overlapping the lower vertical meridian of TO-2 and extending outside presently defined visual field maps, and (3) an activation inferior to hMT+ on the inferotemporal gyrus (ITG) overlapping the parafoveal representation of the TO cluster. This crescent organization of limb-selective activations surrounding hMT+ is reproducible over a span of three years and is consistent across different image types used for localization. Further, these regions exhibit differential position properties: preference for contralateral image presentation decreases and preference for foveal presentation increases from the limb-selective LOS to the MTG. Finally, the relationship between limb-selective activations and visual field maps extends to the dorsal stream where a posterior IPS activation overlaps V7. Overall, our measurements demonstrate a series of LOTC limb-selective activations that 1) have separate anatomical and functional boundaries, 2) overlap distinct visual field maps, and 3) illustrate differential position properties. These findings indicate that category selectivity alone is an insufficient organization principle for defining brain areas. Instead, multiple properties are necessary in order to parcellate and understand the functional organization of high-level visual cortex.
View details for DOI 10.1016/j.neuroimage.2011.03.041
View details for Web of Science ID 000291457500029
View details for PubMedID 21439386
Sparsely-distributed organization of face and limb activations in human ventral temporal cortex
2010; 52 (4): 1559-1573
Functional magnetic resonance imaging (fMRI) has identified face- and body part-selective regions, as well as distributed activation patterns for object categories across human ventral temporal cortex (VTC), eliciting a debate regarding functional organization in VTC and neural coding of object categories. Using high-resolution fMRI, we illustrate that face- and limb-selective activations alternate in a series of largely nonoverlapping clusters in lateral VTC along the inferior occipital gyrus (IOG), fusiform gyrus (FG), and occipito-temporal sulcus (OTS). Both general linear model (GLM) and multivoxel pattern (MVP) analyses show that face- and limb-selective activations minimally overlap and that this organization is consistent across experiments and days. We provide a reliable method to separate two face-selective clusters on the middle and posterior FG (mFus and pFus), and another on the IOG using their spatial relation to limb-selective activations and retinotopic areas hV4, VO-1/2, and hMT+. Furthermore, these activations show a gradient of increasing face selectivity and decreasing limb selectivity from the IOG to the mFus. Finally, MVP analyses indicate that there is differential information for faces in lateral VTC (containing weakly- and highly-selective voxels) relative to non-selective voxels in medial VTC. These findings suggest a sparsely-distributed organization where sparseness refers to the presence of several face- and limb-selective clusters in VTC, and distributed refers to the presence of different amounts of information in highly-, weakly-, and non-selective voxels. Consequently, theories of object recognition should consider the functional and spatial constraints of neural coding across a series of minimally overlapping category-selective clusters that are themselves distributed.
View details for DOI 10.1016/j.neuroimage.2010.04.262
View details for Web of Science ID 000280695200044
View details for PubMedID 20457261
fMRI-Adaptation and Category Selectivity in Human Ventral Temporal Cortex: Regional Differences Across Time Scales
JOURNAL OF NEUROPHYSIOLOGY
2010; 103 (6): 3349-3365
Repeating object images produces stimulus-specific repetition suppression referred to as functional magnetic resonance imaging-adaptation (fMRI-A) in ventral temporal cortex (VTC). However, the effects of stimulus repetition on functional selectivity are largely unknown. We investigated the effects of short-lagged (SL, immediate) and long-lagged (LL, many intervening stimuli) repetitions on category selectivity in VTC using high-resolution fMRI. We asked whether repetition produces scaling or sharpening of fMRI responses both within category-selective regions as well as in the distributed response pattern across VTC. Results illustrate that repetition effects across time scales vary quantitatively along an anterior-posterior axis and qualitatively along a lateral-medial axis. In lateral VTC, both SL and LL repetitions produce proportional fMRI-A with no change in either selectivity or distributed responses as predicted by a scaling model. Further, there is larger fMRI-A in anterior subregions irrespective of category selectivity. Medial VTC exhibits similar scaling effects during SL repetitions. However, for LL repetitions, both the selectivity and distributed pattern of responses vary with category in medial VTC as predicted by a sharpening model. Specifically, there is larger fMRI-A for nonpreferred categories compared with the preferred category, and category selectivity does not predict fMRI-A across the pattern of distributed response. Finally, simulations indicate that different neural mechanisms likely underlie fMRI-A in medial compared to lateral VTC. These results have important implications for future fMRI-A experiments because they suggest that fMRI-A does not reflect a universal neural mechanism and that results of fMRI-A experiments will likely be paradigm independent in lateral VTC but paradigm dependent in medial VTC.
View details for DOI 10.1152/jn.01108.2009
View details for Web of Science ID 000278493900035
View details for PubMedID 20375251
Data on a cytoarchitectonic brain atlas: effects of brain template and a comparison to a multimodal atlas.
Data in brief
2017; 12: 327-332
The data presented here are related to the research article: "A cross-validated cytoarchitectonic atlas of the human ventral visual stream" in which we developed a cytoarchitectonic atlas of ventral visual cortex. Here, we provide two additional quantifications of this cytoarchitectonic atlas: First, we quantify the effect of brain template on cross-validation performance. The data show a comparison between cortex-based alignment to two templates: the postmortem average brain and the FreeSurfer average brain. Second, we quantify the relationship between this cytoarchitectonic atlas and a recently published multimodal atlas of the human brain (Glasser et al., 2016).
View details for DOI 10.1016/j.dib.2017.04.007
View details for PubMedID 28487876
Occipital White Matter Tracts in Human and Macaque.
Cerebral cortex (New York, N.Y. : 1991)
2017; 27 (6): 3346-3359
We compare several major white-matter tracts in human and macaque occipital lobe using diffusion magnetic resonance imaging. The comparison suggests similarities but also significant differences in the tracts. There are several apparently homologous tracts in the 2 species, including the vertical occipital fasciculus (VOF), optic radiation, forceps major, and inferior longitudinal fasciculus (ILF). There is one large human tract, the inferior fronto-occipital fasciculus, with no corresponding fasciculus in macaque. We could identify the macaque VOF (mVOF), which has been little studied. Its position is consistent with classical invasive anatomical studies by Wernicke. VOF homology is supported by similarity of the endpoints in V3A and ventral V4 across species. The mVOF fibers intertwine with the dorsal segment of the ILF, but the human VOF appears to be lateral to the ILF. These similarities and differences between the occipital lobe tracts will be useful in establishing which circuitry in the macaque can serve as an accurate model for human visual cortex.
View details for DOI 10.1093/cercor/bhx070
View details for PubMedID 28369290
Defining the most probable location of the parahippocampal place area using cortex-based alignment and cross-validation.
The parahippocampal place area (PPA) is a widely studied high-level visual region in the human brain involved in place and scene processing. The goal of the present study was to identify the most probable location of place-selective voxels in medial ventral temporal cortex. To achieve this goal, we first used cortex-based alignment (CBA) to create a probabilistic place-selective region of interest (ROI) from one group of 12 participants. We then tested how well this ROI could predict place selectivity in each hemisphere within a new group of 12 participants. Our results reveal that a probabilistic ROI (pROI) generated from one group of 12 participants accurately predicts the location and functional selectivity in individual brains from a new group of 12 participants, despite between subject variability in the exact location of place-selective voxels relative to the folding of parahippocampal cortex. Additionally, the prediction accuracy of our pROI is significantly higher than that achieved by volume-based Talairach alignment. Comparing the location of the pROI of the PPA relative to published data from over 500 participants, including data from the Human Connectome Project, shows a striking convergence of the predicted location of the PPA and the cortical location of voxels exhibiting the highest place selectivity across studies using various methods and stimuli. Specifically, the most predictive anatomical location of voxels exhibiting the highest place selectivity in medial ventral temporal cortex is the junction of the collateral and anterior lingual sulci. Methodologically, we make this pROI freely available (vpnl.stanford.edu/PlaceSelectivity), which provides a means to accurately identify a functional region from anatomical MRI data when fMRI data are not available (for example, in patient populations). Theoretically, we consider different anatomical and functional factors that may contribute to the consistent anatomical location of place selectivity relative to the folding of high-level visual cortex.
View details for DOI 10.1016/j.neuroimage.2017.04.040
View details for PubMedID 28435097
Task alters category representations in prefrontal but not high-level visual cortex.
A central question in neuroscience is how cognitive tasks affect category representations across the human brain. Regions in lateral occipito-temporal cortex (LOTC), ventral temporal cortex (VTC), and ventro-lateral prefrontal cortex (VLFPC) constitute the extended "what" pathway, which is considered instrumental for visual category processing. However, it is unknown (1) whether distributed responses across LOTC, VTC, and VLPFC explicitly represent category, task, or some combination of both, and (2) in what way representations across these subdivisions of the extended 'what' pathway may differ. To fill these gaps in knowledge, we scanned 12 participants using fMRI to test the effect of category and task on distributed responses across LOTC, VTC, and VLPFC. Results reveal that task and category modulate responses in both high-level visual regions, as well as prefrontal cortex. However, we found fundamentally different types of representations across the brain. Distributed responses in high-level visual regions are more strongly driven by category than task, and exhibit task-independent category representations. In contrast, distributed responses in prefrontal cortex are more strongly driven by task than category, and contain task-dependent category representations. Together, these findings of differential representations across the brain support a new idea that LOTC and VTC maintain stable category representations allowing efficient processing of visual information, while prefrontal cortex contains flexible representations in which category information may emerge only when relevant to the task.
View details for DOI 10.1016/j.neuroimage.2017.03.062
View details for PubMedID 28389381
A cross-validated cytoarchitectonic atlas of the human ventral visual stream.
The human ventral visual stream consists of several areas that are considered processing stages essential for perception and recognition. A fundamental microanatomical feature differentiating areas is cytoarchitecture, which refers to the distribution, size, and density of cells across cortical layers. Because cytoarchitectonic structure is measured in 20-micron-thick histological slices of postmortem tissue, it is difficult to assess (a) how anatomically consistent these areas are across brains and (b) how they relate to brain parcellations obtained with prevalent neuroimaging methods, acquired at the millimeter and centimeter scale. Therefore, the goal of this study was to (a) generate a cross-validated cytoarchitectonic atlas of the human ventral visual stream on a whole brain template that is commonly used in neuroimaging studies and (b) to compare this atlas to a recently published retinotopic parcellation of visual cortex (Wang et al., 2014). To achieve this goal, we generated an atlas of eight cytoarchitectonic areas: four areas in the occipital lobe (hOc1-hOc4v) and four in the fusiform gyrus (FG1-FG4), then we tested how the different alignment techniques affect the accuracy of the resulting atlas. Results show that both cortex-based alignment (CBA) and nonlinear volumetric alignment (NVA) generate an atlas with better cross-validation performance than affine volumetric alignment (AVA). Additionally, CBA outperformed NVA in 6/8 of the cytoarchitectonic areas. Finally, the comparison of the cytoarchitectonic atlas to a retinotopic atlas shows a clear correspondence between cytoarchitectonic and retinotopic areas in the ventral visual stream. The successful performance of CBA suggests a coupling between cytoarchitectonic areas and macroanatomical landmarks in the human ventral visual stream, and furthermore, that this coupling can be utilized for generating an accurate group atlas. In addition, the coupling between cytoarchitecture and retinotopy highlights the potential use of this atlas in understanding how anatomical features contribute to brain function. We make this cytoarchitectonic atlas freely available in both BrainVoyager and FreeSurfer formats (http://vpnl.stanford.edu/vcAtlas). The availability of this atlas will enable future studies to link cytoarchitectonic organization to other parcellations of the human ventral visual stream with potential to advance the understanding of this pathway in typical and atypical populations.
View details for DOI 10.1016/j.neuroimage.2017.02.040
View details for PubMedID 28213120
- Two New Cytoarchitectonic Areas on the Human Mid-Fusiform Gyrus CEREBRAL CORTEX 2017; 27 (1): 373-385
The Cytoarchitecture of Domain-specific Regions in Human High-level Visual Cortex.
A fundamental hypothesis in neuroscience proposes that underlying cellular architecture (cytoarchitecture) contributes to the functionality of a brain area. However, this hypothesis has not been tested in human ventral temporal cortex (VTC) that contains domain-specific regions causally involved in perception. To fill this gap in knowledge, we used cortex-based alignment to register functional regions from living participants to cytoarchitectonic areas in ex vivo brains. This novel approach reveals 3 findings. First, there is a consistent relationship between domain-specific regions and cytoarchitectonic areas: each functional region is largely restricted to 1 cytoarchitectonic area. Second, extracting cytoarchitectonic profiles from face- and place-selective regions after back-projecting each region to 20-μm thick histological sections indicates that cytoarchitectonic properties distinguish these regions from each other. Third, some cytoarchitectonic areas contain more than 1 domain-specific region. For example, face-, body-, and character-selective regions are located within the same cytoarchitectonic area. We summarize these findings with a parsimonious hypothesis incorporating how cellular properties may contribute to functional specialization in human VTC. Specifically, we link computational principles to correlated axes of functional and cytoarchitectonic segregation in human VTC, in which parallel processing across domains occurs along a lateral-medial axis while transformations of information within domain occur along an anterior-posterior axis.
View details for PubMedID 27909003
Corresponding ECoG and fMRI category-selective signals in human ventral temporal cortex.
2016; 83: 14-28
Functional magnetic resonance imaging (fMRI) and electrocorticography (ECoG) research have been influential in revealing the functional characteristics of category-selective responses in human ventral temporal cortex (VTC). One important, but unanswered, question is how these two types of measurements might be related with respect to the VTC. Here we examined which components of the ECoG signal correspond to the fMRI response, by using a rare opportunity to measure both fMRI and ECoG responses from the same individuals to images of exemplars of various categories including faces, limbs, cars and houses. Our data reveal three key findings. First, we discovered that the coupling between fMRI and ECoG responses is frequency and time dependent. The strongest and most sustained correlation is observed between fMRI and high frequency broadband (HFB) ECoG responses (30-160hz). In contrast, the correlation between fMRI and ECoG signals in lower frequency bands is temporally transient, where the correlation is initially positive, but then tapers off or becomes negative. Second, we find that the strong and positive correlation between fMRI and ECoG signals in all frequency bands emerges rapidly around 100ms after stimulus onset, together with the onset of the first stimulus-driven neural signals in VTC. Third, we find that the spatial topology and representational structure of category-selectivity in VTC reflected in ECoG HFB responses mirrors the topology and structure observed with fMRI. These findings of a strong and rapid coupling between fMRI and HFB responses validate fMRI measurements of functional selectivity with recordings of direct neural activity and suggest that fMRI category-selective signals in VTC are associated with feed-forward neural processing.
View details for DOI 10.1016/j.neuropsychologia.2015.07.024
View details for PubMedID 26212070
Temporal Processing Capacity in High-Level Visual Cortex Is Domain Specific.
journal of neuroscience
2015; 35 (36): 12412-12424
Prevailing hierarchical models propose that temporal processing capacity-the amount of information that a brain region processes in a unit time-decreases at higher stages in the ventral stream regardless of domain. However, it is unknown if temporal processing capacities are domain general or domain specific in human high-level visual cortex. Using a novel fMRI paradigm, we measured temporal capacities of functional regions in high-level visual cortex. Contrary to hierarchical models, our data reveal domain-specific processing capacities as follows: (1) regions processing information from different domains have differential temporal capacities within each stage of the visual hierarchy and (2) domain-specific regions display the same temporal capacity regardless of their position in the processing hierarchy. In general, character-selective regions have the lowest capacity, face- and place-selective regions have an intermediate capacity, and body-selective regions have the highest capacity. Notably, domain-specific temporal processing capacities are not apparent in V1 and have perceptual implications. Behavioral testing revealed that the encoding capacity of body images is higher than that of characters, faces, and places, and there is a correspondence between peak encoding rates and cortical capacities for characters and bodies. The present evidence supports a model in which the natural statistics of temporal information in the visual world may affect domain-specific temporal processing and encoding capacities. These findings suggest that the functional organization of high-level visual cortex may be constrained by temporal characteristics of stimuli in the natural world, and this temporal capacity is a characteristic of domain-specific networks in high-level visual cortex.Visual stimuli bombard us at different rates every day. For example, words and scenes are typically stationary and vary at slow rates. In contrast, bodies are dynamic and typically change at faster rates. Using a novel fMRI paradigm, we measured temporal processing capacities of functional regions in human high-level visual cortex. Contrary to prevailing theories, we find that different regions have different processing capacities, which have behavioral implications. In general, character-selective regions have the lowest capacity, face- and place-selective regions have an intermediate capacity, and body-selective regions have the highest capacity. These results suggest that temporal processing capacity is a characteristic of domain-specific networks in high-level visual cortex and contributes to the segregation of cortical regions.
View details for DOI 10.1523/JNEUROSCI.4822-14.2015
View details for PubMedID 26354910
Attention reduces spatial uncertainty in human ventral temporal cortex.
2015; 25 (5): 595-600
Ventral temporal cortex (VTC) is the latest stage of the ventral "what" visual pathway, which is thought to code the identity of a stimulus regardless of its position or size [1, 2]. Surprisingly, recent studies show that position information can be decoded from VTC [3-5]. However, the computational mechanisms by which spatial information is encoded in VTC are unknown. Furthermore, how attention influences spatial representations in human VTC is also unknown because the effect of attention on spatial representations has only been examined in the dorsal "where" visual pathway [6-10]. Here, we fill these significant gaps in knowledge using an approach that combines functional magnetic resonance imaging and sophisticated computational methods. We first develop a population receptive field (pRF) model [11, 12] of spatial responses in human VTC. Consisting of spatial summation followed by a compressive nonlinearity, this model accurately predicts responses of individual voxels to stimuli at any position and size, explains how spatial information is encoded, and reveals a functional hierarchy in VTC. We then manipulate attention and use our model to decipher the effects of attention. We find that attention to the stimulus systematically and selectively modulates responses in VTC, but not early visual areas. Locally, attention increases eccentricity, size, and gain of individual pRFs, thereby increasing position tolerance. However, globally, these effects reduce uncertainty regarding stimulus location and actually increase position sensitivity of distributed responses across VTC. These results demonstrate that attention actively shapes and enhances spatial representations in the ventral visual pathway.
View details for DOI 10.1016/j.cub.2014.12.050
View details for PubMedID 25702580
View details for PubMedCentralID PMC4348205
Electrical stimulation of the left and right human fusiform gyrus causes different effects in conscious face perception.
journal of neuroscience
2014; 34 (38): 12828-12836
Neuroimaging and electrophysiological studies across species have confirmed bilateral face-selective responses in the ventral temporal cortex (VTC) and prosopagnosia is reported in patients with lesions in the VTC including the fusiform gyrus (FG). As imaging and electrophysiological studies provide correlative evidence, and brain lesions often comprise both white and gray matter structures beyond the FG, we designed the current study to explore the link between face-related electrophysiological responses in the FG and the causal effects of electrical stimulation of the left or right FG in face perception. We used a combination of electrocorticography (ECoG) and electrical brain stimulation (EBS) in 10 human subjects implanted with intracranial electrodes in either the left (5 participants, 30 FG sites) or right (5 participants, 26 FG sites) hemispheres. We identified FG sites with face-selective ECoG responses, and recorded perceptual reports during EBS of these sites. In line with existing literature, face-selective ECoG responses were present in both left and right FG sites. However, when the same sites were stimulated, we observed a striking difference between hemispheres. Only EBS of the right FG caused changes in the conscious perception of faces, whereas EBS of strongly face-selective regions in the left FG produced non-face-related visual changes, such as phosphenes. This study examines the relationship between correlative versus causal nature of ECoG and EBS, respectively, and provides important insight into the differential roles of the right versus left FG in conscious face perception.
View details for DOI 10.1523/JNEUROSCI.0527-14.2014
View details for PubMedID 25232118
- Electrical Stimulation of the Left and Right Human Fusiform Gyrus Causes Different Effects in Conscious Face Perception JOURNAL OF NEUROSCIENCE 2014; 34 (38): 12828-12836
Neural representations of faces and limbs neighbor in human high-level visual cortex: evidence for a new organization principle
PSYCHOLOGICAL RESEARCH-PSYCHOLOGISCHE FORSCHUNG
2013; 77 (1): 74-97
Neurophysiology and optical imaging studies in monkeys and functional magnetic resonance imaging (fMRI) studies in both monkeys and humans have localized clustered neural responses in inferotemporal cortex selective for images of biologically relevant categories, such as faces and limbs. Using higher resolution (1.5 mm voxels) fMRI scanning methods than past studies (3-5 mm voxels), we recently reported a network of multiple face- and limb-selective regions that neighbor one another in human ventral temporal cortex (Weiner and Grill-Spector, Neuroimage, 52(4):1559-1573, 2010) and lateral occipitotemporal cortex (Weiner and Grill-Spector, Neuroimage, 56(4):2183-2199, 2011). Here, we expand on three basic organization principles of high-level visual cortex revealed by these findings: (1) consistency in the anatomical location of functional regions, (2) preserved spatial relationship among functional regions, and (3) a topographic organization of face- and limb-selective regions in adjacent and alternating clusters. We highlight the implications of this structure in comparing functional brain organization between typical and atypical populations. We conclude with a new model of high-level visual cortex consisting of ventral, lateral, and dorsal components, where multimodal processing related to vision, action, haptics, and language converges in the lateral pathway.
View details for DOI 10.1007/s00426-011-0392-x
View details for Web of Science ID 000313053700008
View details for PubMedID 22139022
Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception
JOURNAL OF NEUROSCIENCE
2012; 32 (43): 14915-14920
Face-selective neural responses in the human fusiform gyrus have been widely examined. However, their causal role in human face perception is largely unknown. Here, we used a multimodal approach of electrocorticography (ECoG), high-resolution functional magnetic resonance imaging (fMRI), and electrical brain stimulation (EBS) to directly investigate the causal role of face-selective neural responses of the fusiform gyrus (FG) in face perception in a patient implanted with subdural electrodes in the right inferior temporal lobe. High-resolution fMRI identified two distinct FG face-selective regions [mFus-faces and pFus-faces (mid and posterior fusiform, respectively)]. ECoG revealed a striking anatomical and functional correspondence with fMRI data where a pair of face-selective electrodes, positioned 1 cm apart, overlapped mFus-faces and pFus-faces, respectively. Moreover, electrical charge delivered to this pair of electrodes induced a profound face-specific perceptual distortion during viewing of real faces. Specifically, the subject reported a "metamorphosed" appearance of faces of people in the room. Several controls illustrate the specificity of the effect to the perception of faces. EBS of mFus-faces and pFus-faces neither produced a significant deficit in naming pictures of famous faces on the computer, nor did it affect the appearance of nonface objects. Further, the appearance of faces remained unaffected during both sham stimulation and stimulation of a pair of nearby electrodes that were not face-selective. Overall, our findings reveal a striking convergence of fMRI, ECoG, and EBS, which together offer a rare causal link between functional subsets of the human FG network and face perception.
View details for DOI 10.1523/JNEUROSCI.2609-12.2012
View details for Web of Science ID 000310523900008
View details for PubMedID 23100414
- Synchrony upon repetition: One or multiple neural mechanisms? COGNITIVE NEUROSCIENCE 2012; 3 (3-4): 243-244
Illusions of Visual Motion Elicited by Electrical Stimulation of Human MT Complex
2011; 6 (7)
Human cortical area MT(+) (hMT(+)) is known to respond to visual motion stimuli, but its causal role in the conscious experience of motion remains largely unexplored. Studies in non-human primates demonstrate that altering activity in area MT can influence motion perception judgments, but animal studies are inherently limited in assessing subjective conscious experience. In the current study, we use functional magnetic resonance imaging (fMRI), intracranial electrocorticography (ECoG), and electrical brain stimulation (EBS) in three patients implanted with intracranial electrodes to address the role of area hMT(+) in conscious visual motion perception. We show that in conscious human subjects, reproducible illusory motion can be elicited by electrical stimulation of hMT(+). These visual motion percepts only occurred when the site of stimulation overlapped directly with the region of the brain that had increased fMRI and electrophysiological activity during moving compared to static visual stimuli in the same individual subjects. Electrical stimulation in neighboring regions failed to produce illusory motion. Our study provides evidence for the sufficient causal link between the hMT(+) network and the human conscious experience of visual motion. It also suggests a clear spatial relationship between fMRI signal and ECoG activity in the human brain.
View details for DOI 10.1371/journal.pone.0021798
View details for Web of Science ID 000292781500016
View details for PubMedID 21765915
Neural Representations of Faces and Body Parts in Macaque and Human Cortex: A Comparative fMRI Study
JOURNAL OF NEUROPHYSIOLOGY
2009; 101 (5): 2581-2600
Single-cell studies in the macaque have reported selective neural responses evoked by visual presentations of faces and bodies. Consistent with these findings, functional magnetic resonance imaging studies in humans and monkeys indicate that regions in temporal cortex respond preferentially to faces and bodies. However, it is not clear how these areas correspond across the two species. Here, we directly compared category-selective areas in macaques and humans using virtually identical techniques. In the macaque, several face- and body part-selective areas were found located along the superior temporal sulcus (STS) and middle temporal gyrus (MTG). In the human, similar to previous studies, face-selective areas were found in ventral occipital and temporal cortex and an additional face-selective area was found in the anterior temporal cortex. Face-selective areas were also found in lateral temporal cortex, including the previously reported posterior STS area. Body part-selective areas were identified in the human fusiform gyrus and lateral occipitotemporal cortex. In a first experiment, both monkey and human subjects were presented with pictures of faces, body parts, foods, scenes, and man-made objects, to examine the response profiles of each category-selective area to the five stimulus types. In a second experiment, face processing was examined by presenting upright and inverted faces. By comparing the responses and spatial relationships of the areas, we propose potential correspondences across species. Adjacent and overlapping areas in the macaque anterior STS/MTG responded strongly to both faces and body parts, similar to areas in the human fusiform gyrus and posterior STS. Furthermore, face-selective areas on the ventral bank of the STS/MTG discriminated both upright and inverted faces from objects, similar to areas in the human ventral temporal cortex. Overall, our findings demonstrate commonalities and differences in the wide-scale brain organization between the two species and provide an initial step toward establishing functionally homologous category-selective areas.
View details for DOI 10.1152/jn.91198.2008
View details for Web of Science ID 000265398100038
View details for PubMedID 19225169
Topographic maps in human frontal cortex revealed in memory-guided saccade and spatial working-memory tasks
JOURNAL OF NEUROPHYSIOLOGY
2007; 97 (5): 3494-3507
We used fMRI at 3 Tesla and improved spatial resolution (2 x 2 x 2 mm(3)) to investigate topographic organization in human frontal cortex using memory-guided response tasks performed at 8 or 12 peripheral locations arranged clockwise around a central fixation point. The tasks required the location of a peripheral target to be remembered for several seconds after which the subjects either made a saccade to the remembered location (memory-guided saccade task) or judged whether a test stimulus appeared in the same or a slightly different location by button press (spatial working-memory task). With these tasks, we found two topographic maps in each hemisphere, one in the superior branch of precentral cortex and caudalmost part of the superior frontal sulcus, in the region of the human frontal eye field, and a second in the inferior branch of precentral cortex and caudalmost part of the inferior frontal sulcus, both of which greatly overlapped with activations evoked by visually guided saccades. In each map, activated voxels coded for saccade directions and memorized locations predominantly in the contralateral hemifield with neighboring saccade directions and memorized locations represented in adjacent locations of the map. Particular saccade directions or memorized locations were often represented in multiple locations of the map. The topographic activation patterns showed individual variability from subject to subject but were reproducible within subjects. Notably, only saccade-related activation, but no topographic organization, was found in the region of the human supplementary eye field in dorsomedial prefrontal cortex. Together these results show that topographic organization can be revealed outside sensory cortical areas using more complex behavioral tasks.
View details for DOI 10.1152/jn.00010.2007
View details for Web of Science ID 000247933500032
View details for PubMedID 17360822