Human High-level Visual Cortex Research Articles

Better models of human high-level visual cortex emerge from natural language supervision with a large and diverse dataset

Better models of human high-level visual cortex emerge from natural language supervision with a large and diverse dataset

Maps of object animacy and aspect ratio in human high-level visual cortex.

Maps of object animacy and aspect ratio in human high-level visual cortex.

Causal Evidence for a Double Dissociation between Object- and Scene-Selective Regions of Visual Cortex: A Preregistered TMS Replication Study.

Natural scenes are characterized by individual objects as well as by global scene properties such as spatial layout. Functional neuroimaging research has shown that this distinction between object and scene processing is one of the main organizing principles of human high-level visual cortex. For example, object-selective regions, including the lateral occipital complex (LOC), were shown to represent object content (but not scene layout), while scene-selective regions, including the occipital place area (OPA), were shown to represent scene layout (but not object content). Causal evidence for a double dissociation between LOC and OPA in representing objects and scenes is currently limited, however. One TMS experiment, conducted in a relatively small sample (N = 13), reported an interaction between LOC and OPA stimulation and object and scene recognition performance (Dilks et al., 2013). Here, we present a high-powered preregistered replication of this study (N = 72, including male and female human participants), using group-average fMRI coordinates to target LOC and OPA. Results revealed unambiguous evidence for a double dissociation between LOC and OPA: relative to vertex stimulation, TMS over LOC selectively impaired the recognition of objects, while TMS over OPA selectively impaired the recognition of scenes. Furthermore, we found that these effects were stable over time and consistent across individual objects and scenes. These results show that LOC and OPA can be reliably and selectively targeted with TMS, even when defined based on group-average fMRI coordinates. More generally, they support the distinction between object and scene processing as an organizing principle of human high-level visual cortex.SIGNIFICANCE STATEMENT Our daily-life environments are characterized both by individual objects and by global scene properties. The distinction between object and scene processing features prominently in visual cognitive neuroscience, with fMRI studies showing that this distinction is one of the main organizing principles of human high-level visual cortex. However, causal evidence for the selective involvement of object- and scene-selective regions in processing their preferred category is less conclusive. Here, testing a large sample (N = 72) using an established paradigm and a preregistered protocol, we found that TMS over object-selective cortex (lateral occipital complex) selectively impaired object recognition, while TMS over scene-selective cortex (occipital place area) selectively impaired scene recognition. These results provide strong causal evidence for the distinction between object and scene processing in human visual cortex.

Extensive childhood experience with Pokémon suggests eccentricity drives organization of visual cortex.

The functional organization of human high-level visual cortex, such as the face- and place-selective regions, is strikingly consistent across individuals. An unanswered question in neuroscience concerns which dimensions of visual information constrain the development and topography of this shared brain organization. To answer this question, we used functional magnetic resonance imaging to scan a unique group of adults who, as children, had extensive visual experience with Pokémon. These animal-like, pixelated characters are dissimilar from other ecological categories, such as faces and places, along critical dimensions (foveal bias, rectilinearity, size, animacy). We show not only that adults who have Pokémon experience demonstrate distinct distributed cortical responses to Pokémon, but also that the experienced retinal eccentricity during childhood can predict the locus of Pokémon responses in adulthood. These data demonstrate that inherent functional representations in the visual cortex-retinal eccentricity-combined with consistent viewing behaviour of particular stimuli during childhood result in a shared functional topography in adulthood.

MEG sensor patterns reflect perceptual but not categorical similarity of animate and inanimate objects

Human high-level visual cortex shows a distinction between animate and inanimate objects, as revealed by fMRI. Recent studies have shown that object animacy can similarly be decoded from MEG sensor patterns. Which object properties drive this decoding? Here, we disentangled the influence of perceptual and categorical object properties by presenting perceptually matched objects (e.g., snake and rope) that were nonetheless easily recognizable as being animate or inanimate. In a series of behavioral experiments, three aspects of perceptual dissimilarity of these objects were quantified: overall dissimilarity, outline dissimilarity, and texture dissimilarity. Neural dissimilarity of MEG sensor patterns was modeled using regression analysis, in which perceptual dissimilarity (from the behavioral experiments) and categorical dissimilarity served as predictors of neural dissimilarity. We found that perceptual dissimilarity was strongly reflected in MEG sensor patterns from 80 ms after stimulus onset, with separable contributions of outline and texture dissimilarity. Surprisingly, when controlling for perceptual dissimilarity, MEG patterns did not carry information about object category (animate vs inanimate) at any time point. Nearly identical results were found in a second MEG experiment that required basic-level object recognition. This is in contrast to results observed in fMRI using the same stimuli, task, and analysis approach: fMRI voxel patterns in object-selective cortex showed a highly reliable categorical distinction even when controlling for perceptual dissimilarity. These results suggest that MEG sensor patterns do not capture object animacy independently of perceptual differences between animate and inanimate objects.

Eccentricity drives developmental organization of human high-level visual cortex

Eccentricity drives developmental organization of human high-level visual cortex

Large-Scale Organization of the Hand Action Observation Network in Individuals Born Without Hands.

The human high-level visual cortex comprises regions specialized for the processing of distinct types of stimuli, such as objects, animals, and human actions. How does this specialization emerge? Here, we investigated the role of effector-specific visuomotor coupling experience in shaping the organization of the action observation network (AON) as a window on this question. Observed body movements are frequently coupled with corresponding motor codes, e.g., during monitoring one's own movements and imitation, resulting in bidirectionally connected circuits between areas involved in body movements observation (e.g., of the hand) and the motor codes involved in their execution. If the organization of the AON is shaped by this effector-specific visuomotor coupling, then, it should not form for body movements that do not belong to individuals' motor repertoire. To test this prediction, we used fMRI to investigate the spatial arrangement and functional properties of the hand and foot action observation circuits in individuals born without upper limbs. Multivoxel pattern decoding, pattern similarity, and univariate analyses revealed an intact hand AON in the individuals born without upper limbs. This suggests that the organization of the AON does not require effector-specific visuomotor coupling.

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.

Macromolecular proliferation in human high-level visual cortex constrains development of function and behavior

Macromolecular proliferation in human high-level visual cortex constrains development of function and behavior

Temporal Processing Capacity in High-Level Visual Cortex Is Domain Specific.

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. Significance statement: 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.

Differential rate of temporal processing across category-selective regions in human high-level visual cortex

What is the speed of processing in high-level visual cortex? Previous research (McKeeff et al. 2007) suggests that responses in human face- and scene-selective regions peak for stimuli presented at 4-5 Hz, unlike early visual areas that respond maximally for faster rates of presentation (18-25 Hz). However, these results are hard to interpret because presentation rate and the number of images in a block were confounded. Here, we used a novel paradigm to measure the rate of processing across human high-level category-selective regions. Twelve participants were scanned with fMRI while viewing images of faces, bodies, objects, scenes, and written characters presented at 1, 2, 4, or 8 Hz. Stimuli were presented in 8-image blocks at all rates to equalize the number of stimuli in a block across rates. Results indicate that networks of category-selective regions are optimized to process stimuli at different rates, with regions selective for faces, scenes, and characters preferring slower rates (2 Hz), and body-selective regions preferring faster rates (4 & 8 Hz). This pattern of results manifests in three ways: (i) The proportion of VTC voxels showing selectivity for a category peaked at a certain rate. Specifically, the proportion of VTC voxels selective for faces, scenes, and characters was greatest at 2 Hz, and the proportion selective for body parts was greatest at 4 Hz (Figure 1). (ii) Independent ROI analyses revealed that selectivity for the preferred category was highest at the optimal rate associated with a region. (iii) Heightened selectivity resulted from a specific increase in the magnitude of response to a region's preferred category at the optimal rate. These results demonstrate differential temporal processing of category information across high-level visual cortex and that bodies are processed at faster rates than other types of stimuli, perhaps as a result of their mobility and non-rigid nature. Meeting abstract presented at VSS 2014

High-resolution fMRI reveals cortical tiling of face and limb selectivity in human high-level visual cortex

High-resolution fMRI reveals cortical tiling of face and limb selectivity in human high-level visual cortex

Representation of possible and impossible objects in the human visual cortex: Evidence from fMRI adaptation

Impossible objects are defined as 2D drawings that represent objects that could not exist in real 3D space. Previous studies have proposed that such objects are represented differently in long-term memory due to their invalid spatial structure. Nevertheless, it is not clear whether these discrepancies reflect early perceptual processes or late, post-recognition, processes. Here, we address this issue by using fMRI adaptation. Interestingly, equivalent adaptation levels were obtained for repeated compared to non-repeated possible and impossible objects in object selective regions within the human high-level visual cortex. Yet, a significant correlation between fMRI adaptation and behavioral facilitation was found for possible but not for impossible objects, thus exhibiting some dissociation in the representation of the two object categories. Overall, our findings suggest that the initial perception of possible and impossible objects is mediated by shared neural mechanisms whereas the observed differences between the two types of objects may reflect higher post-recognition processes.

Parametric face-to-hand transformations reveal shape-tuned representations in human high-level visual cortex.

Parametric face-to-hand transformations reveal shape-tuned representations in human high-level visual cortex.

Neural representations of faces and limbs neighbor in human high-level visual cortex: evidence for a new organization principle

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.Electronic supplementary materialThe online version of this article (doi:10.1007/s00426-011-0392-x) contains supplementary material, which is available to authorized users.

Mirror-image confusion in human high-level visual cortex

Mirror-image confusion in human high-level visual cortex