Two hierarchically organized neural systems for object information in human visual cortex

The primate visual system is broadly organized into two segregated processing pathways, a ventral stream for object vision and a dorsal stream for space vision. Here, evidence from functional brain imaging in humans demonstrates that object representations are not confined to the ventral pathway, but can also be found in several areas along the dorsal pathway. In both streams, areas at intermediate processing stages in extrastriate cortex (V4, V3A, MT and V7) showed object-selective but viewpoint- and size-specific responses. In contrast, higher-order areas in lateral occipital and posterior parietal cortex (LOC, IPS1 and IPS2) responded selectively to objects independent of image transformations. Contrary to the two-pathways hypothesis, our findings indicate that basic object information related to shape, size and viewpoint may be represented similarly in two parallel and hierarchically organized neural systems in the ventral and dorsal visual pathways.     

Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas

Although both reaching and grasping require transporting the hand to the object location, only grasping also requires processing of object shape, size and orientation to preshape the hand. Behavioural and neuropsychological evidence suggests that the object processing required for grasping relies on different neural substrates from those mediating object recognition. Specifically, whereas object recognition is believed to rely on structures in the ventral (occipitotemporal) stream, object grasping appears to rely on structures in the dorsal (occipitoparietal) stream. We used functional magnetic resonance imaging (fMRI) to determine whether grasping (compared to reaching) produced activation in dorsal areas, ventral areas, or both. We found greater activity for grasping than reaching in several regions, including anterior intraparietal (AIP) cortex. We also performed a standard object perception localizer (comparing intact vs. scrambled 2D object images) in the same subjects to identify the lateral occipital complex (LOC), a ventral stream area believed to play a critical role in object recognition. Although LOC was activated by the objects presented on both grasping and reaching trials, there was no greater activity for grasping compared to reaching. These results suggest that dorsal areas, including AIP, but not ventral areas such as LOC, play a fundamental role in computing object properties during grasping.     

A model of V4 shape selectivity and invariance

Object recognition in primates is mediated by the ventral visual pathway and is classically described as a feedforward hierarchy of increasingly sophisticated representations. Neurons in macaque monkey area V4, an intermediate stage along the ventral pathway, have been shown to exhibit selectivity to complex boundary conformation and invariance to spatial translation. How could such a representation be derived from the signals in lower visual areas such as V1? We show that a quantitative model of hierarchical processing, which is part of a larger model of object recognition in the ventral pathway, provides a plausible mechanism for the translation-invariant shape representation observed in area V4. Simulated model neurons successfully reproduce V4 selectivity and invariance through a nonlinear, translation-invariant combination of locally selective subunits, suggesting that a similar transformation may occur or culminate in area V4. Specifically, this mechanism models the selectivity of individual V4 neurons to boundary conformation stimuli, exhibits the same degree of translation invariance observed in V4, and produces observed V4 population responses to bars and non-Cartesian gratings. This work provides a quantitative model of the widely described shape selectivity and invariance properties of area V4 and points toward a possible canonical mechanism operating throughout the ventral pathway.     

Temporal limitations in object processing across the human ventral visual pathway

Behavioral studies have shown that object recognition becomes severely impaired at fast presentation rates, indicating a limitation in temporal processing capacity. Here, we studied whether this behavioral limit in object recognition reflects limitations in the temporal processing capacity of early visual areas tuned to basic features or high-level areas tuned to complex objects. We used functional MRI (fMRI) to measure the temporal processing capacity of multiple areas along the ventral visual pathway progressing from the primary visual cortex (V1) to high-level object-selective regions, specifically the fusiform face area (FFA) and parahippocampal place area (PPA). Subjects viewed successive images of faces or houses at presentation rates varying from 2.3 to 37.5 items/s while performing an object discrimination task. Measures of the temporal frequency response profile of each visual area revealed a systematic decline in peak tuning across the visual hierarchy. Areas V1-V3 showed peak activity at rapid presentation rates of 18-25 items/s, area V4v peaked at intermediate rates (9 items/s), and the FFA and PPA peaked at the slowest temporal rates (4-5 items/s). Our results reveal a progressive loss in the temporal processing capacity of the human visual system as information is transferred from early visual areas to higher areas. These data suggest that temporal limitations in object recognition likely result from the limited processing capacity of high-level object-selective areas rather than that of earlier stages of visual processing.     

Neural correlates of disparity-defined shape discrimination in the human brain

Binocular disparity, the slight differences between the images registered by our two eyes, provides an important cue when estimating the three-dimensional (3D) structure of the complex environment we inhabit. Sensitivity to binocular disparity is evident at multiple levels of the visual hierarchy in the primate brain, from early visual cortex to parietal and temporal areas. However, the relationship between activity in these areas and key perceptual functions that exploit disparity information for 3D shape perception remains an important open question. Here we investigate the link between human cortical activity and the perception of disparity-defined shape, measuring fMRI responses concurrently with psychophysical shape judgments. We parametrically degraded the coherence of shapes by shuffling the spatial position of dots whose disparity defined the 3D structure and investigated the effect of this stimulus manipulation on both cortical activity and shape discrimination. We report significant relationships between shape coherence and fMRI response in both dorsal (V3, hMT+/V5) and ventral (LOC) visual areas that correspond to the observers' discrimination performance. In contrast to previous suggestions of a dichotomy of disparity-related processes in the ventral and dorsal streams, these findings are consistent with proposed interactions between these pathways that may mediate a continuum of processes important in perceiving 3D shape from coarse contour segmentation to fine curvature estimation.     

Visuo-haptic object-related activation in the ventral visual pathway

The ventral pathway is involved in primate visual object recognition. In humans, a central stage in this pathway is an occipito-temporal region termed the lateral occipital complex (LOC), which is preferentially activated by visual objects compared to scrambled images or textures. However, objects have characteristic attributes (such as three-dimensional shape) that can be perceived both visually and haptically. Therefore, object-related brain areas may hold a representation of objects in both modalities. Using fMRI to map object-related brain regions, we found robust and consistent somatosensory activation in the occipito-temporal cortex. This region showed clear preference for objects compared to textures in both modalities. Most somatosensory object-selective voxels overlapped a part of the visual object-related region LOC. Thus, we suggest that neuronal populations in the occipito-temporal cortex may constitute a multimodal object-related network.     

Projections from the cytochrome oxidase modules of visual area V2 to the ventral posterior area in the macaque

The ventral part of the third visual cortical complex, the ventral posterior area (VP) or V3v, is located between the ventral half of visual areas V2 and V4. Because of its location and the physiological properties of its neurons, VP has been considered to be involved in the ventral stream visual areas. The ventral stream visual areas such as V4 and TEO receive projections from the cytochrome oxidase (CO)-rich thin stripes and CO-poor interstripe regions of V2; however, which CO-modules project to VP remains unclear. Moreover, it is not clear whether V1 projects to VP. We injected retrograde tracers into VP and found that VP receives projections from V2 neurons not only in the CO-rich thin stripes and CO-poor interstripe regions but also in the CO-rich thick stripes. We also confirmed the virtual absence of inputs from V1 to VP. These results support the hypothesis that VP constitutes a distinct extrastriate visual area and also suggest that, in addition to color and shape information, VP may also process visual information related to space and disparity.     

Implied motion from form in the human visual cortex

When cartoonists use speed lines--also called motion streaks--to suggest the speed of a stationary object, they use form to imply motion. The goal of this study was to investigate the mechanisms that mediate the percept of implied motion in the human visual cortex. In an adaptation functional imaging paradigm we presented Glass patterns that, just like speed lines, imply motion but do not on average contain coherent motion energy. We found selective adaptation to these patterns in the human motion complex, the lateral occipital complex (LOC), and earlier visual areas. Glass patterns contain both local orientation features and global structure. To disentangle these aspects we performed a control experiment using Glass patterns with minimal local orientation differences but large global structure differences. This experiment showed that selectivity for Glass patterns arises in part in areas beyond V1 and V2. Interestingly, the selective adaptation transferred from implied motion stimuli to similar real motion patterns in dorsal but not ventral areas. This suggests that the same subpopulations of cells in dorsal areas that are selective for implied motion are also selective for real motion. In other words, these cells are invariant with respect to the cue (implied or real) that generates the motion. We conclude that the human motion complex responds to Glass patterns as if they contain coherent motion. This, presumably, is the reason why these patterns appear to move coherently. The LOC, however, has different cells that respond to the structure of real motion patterns versus implied motion patterns. Such a differential response may allow ventral areas to further analyze the structure of global patterns.     

Perceptual continuity and the emergence of perceptual persistence in the ventral visual pathway

Perceptual continuity is an important aspect of our experience of the visual world. In this study, we focus on an example of perceptual continuity involving the maintenance of figure-ground segregation despite the removal of binding cues that initiated the segregation. Fragmented line drawings of objects were superimposed on a background of randomly oriented lines. Global forms could be discriminated from the background based on differences in motion or differences in color/brightness. Furthermore, perception of a global form persisted after the binding cue had been removed. A comparison between the persistence of forms constructed from motion or color demonstrated that both forms produced persistence after the object defining cues were removed. Functional imaging showed a gradual increase in the persistence of brain activity in the lower visual areas (V1, V2, VP), which reached significance in V4v and peaked in the lateral occipital area. There was no difference in the location of persistence for color- or motion-defined forms. These results suggest that the retention of a global percept is an emerging property of the ventral visual processing stream and the maintenance of grouped visual elements is independent of cue type. We postulated that perceptual persistence depends on a system of perceptual memory reflecting the state of perceptual organization.     

Frequency-Following and Connectivity of Different Visual Areas in Response to Contrast-Reversal Stimulation

The sensitivity of visual areas to different temporal frequencies, as well as the functional connections between these areas, was examined using magnetoencephalography (MEG). Alternating circular sinusoids (0, 3.1, 8.7 and 14 Hz) were presented to foveal and peripheral locations in the visual field to target ventral and dorsal stream structures, respectively. It was hypothesized that higher temporal frequencies would preferentially activate dorsal stream structures. To determine the effect of frequency on the cortical response we analyzed the late time interval (220–770 ms) using a multi-dipole spatio-temporal analysis approach to provide source locations and timecourses for each condition. As an exploratory aspect, we performed cross-correlation analysis on the source timecourses to determine which sources responded similarly within conditions. Contrary to predictions, dorsal stream areas were not activated more frequently during high temporal frequency stimulation. However, across cortical sources the frequency-following response showed a difference, with significantly higher power at the second harmonic for the 3.1 and 8.7 Hz stimulation and at the first and second harmonics for the 14 Hz stimulation with this pattern seen robustly in area V1. Cross-correlations of the source timecourses showed that both low- and high-order visual areas, including dorsal and ventral stream areas, were significantly correlated in the late time interval. The results imply that frequency information is transferred to higher-order visual areas without translation. Despite the less complex waveforms seen in the late interval of time, the cross-correlation results show that visual, temporal and parietal cortical areas are intricately involved in late-interval visual processing.     

Differential development of high-level visual cortex correlates with category-specific recognition memory

High-level visual cortex in humans includes functionally defined regions that preferentially respond to objects, faces and places. It is unknown how these regions develop and whether their development relates to recognition memory. We used functional magnetic resonance imaging to examine the development of several functionally defined regions including object (lateral occipital complex, LOC)-, face ('fusiform face area', FFA; superior temporal sulcus, STS)- and place ('parahippocampal place area', PPA)-selective cortices in children (ages 7-11), adolescents (12-16) and adults. Right FFA and left PPA volumes were substantially larger in adults than in children. This development occurred by expansion of FFA and PPA into surrounding cortex and was correlated with improved recognition memory for faces and places, respectively. In contrast, LOC and STS volumes and object-recognition memory remained constant across ages. Thus, the ventral stream undergoes a prolonged maturation that varies temporally across functional regions, is determined by brain region rather than stimulus category, and is correlated with the development of category-specific recognition memory.     

Spontaneous in-flight accommodation of hand orientation to unseen grasp targets: A case of action blindsight

The division of labour between the dorsal and ventral visual pathways is well established. The ventral stream supports object identification, while the dorsal stream supports online processing of visual information in the service of visually guided actions. Here, we report a case of an individual with a right inferior quadrantanopia who exhibited accurate spontaneous rotation of his wrist when grasping a target object in his blind visual field. His accurate wrist orientation was observed despite the fact that he exhibited no sensitivity to the orientation of the handle in a perceptual matching task. These findings indicate that non-geniculostriate visual pathways process basic volumetric information relevant to grasping, and reinforce the observation that phenomenal awareness is not necessary for an object’s volumetric properties to influence visuomotor performance.     

Graded size sensitivity of object-exemplar-evoked activity patterns within human LOC subregions

A central issue for understanding visual object recognition is how the cortical hierarchy represents incoming sensory information and transforms it across successive processing stages. The format of object representation in the human brain has thus far mostly been studied using adaptation paradigms because the neuronal layout of object selectivities was thought to be beyond the resolution of conventional functional MRI (fMRI). Recently, however, multivariate pattern recognition succeeded in discriminating fMRI responses of object-selective cortex to different object exemplars within a given category. Here, we use increased spatial fMRI resolution to explore size sensitivity and tolerance to size change of response patterns evoked by object exemplars across a range of three sizes. Results from Support Vector Classification on responses of the human lateral occipital complex (LOC) show that discrimination of size (for a given object) and discrimination of objects across changes in size depended on the amount of size difference. Even across the largest amount of size change, accuracy for generalization was still significant in LOC, whereas the same comparison was at chance performance in early visual (calcarine) cortex. Analyzing subregions, we further found an anterior-posterior gradient in the degree of size sensitivity and size generalization within the posterior-dorsal and anterior-ventral parts of LOC. These results speak against fully size-invariant representation of object information in human LOC and are hence congruent with findings in monkeys showing object identity and size information in population activity of inferotemporal cortex. Moreover, these results provide evidence for a fine-grained functional heterogeneity within human LOC beyond the commonly used LO/fusiform subdivision.     

Color sensitivity of cells responsive to complex stimuli in the temporal cortex

The inferotemporal (IT) cortex of the monkey lies at the head of the ventral visual pathway and is known to mediate object recognition and discrimination. It is often assumed that color plays a minor role in the recognition of objects and faces because discrimination remains highly accurate with black-and-white images. Furthermore it has been suggested that for rapid presentation and reaction tasks, object classification may be based on a first wave of feedforward visual information, which is coarse and achromatic. The fine detail and color information follows later, allowing similar stimuli to be discriminated. To allow these theories to be tested, this study investigates whether the presence of color affects the response of IT neurons to complex stimuli, such as faces, and whether color information is delayed with respect to information about stimulus form in these cells. Color, achromatic, and false-color versions of effective stimuli were presented using a rapid serial visual presentation paradigm, and responses recorded from single cells in IT of the adult monkey. Achromatic images were found to evoke significantly reduced responses compared with color images in the majority of neurons (70%) tested. Differential activity for achromatic and colored stimuli was evident from response onset with no evidence to support the hypothesis that information about object color is delayed with respect to object form. A negative correlation (P < 0.01) was found between cell latency and color sensitivity, with the most color-sensitive cells tending to respond earliest. The results of this study suggest a strong role for color in familiar object recognition and provide no evidence to support the idea of a first wave of form processing in the ventral stream based on purely achromatic information.     

A Putative Model of Multisensory Object Representation

This review surveys the recent literature on visuo-haptic convergence in the perception of object form, with particular reference to the lateral occipital complex (LOC) and the intraparietal sulcus (IPS) and discusses how visual imagery or multisensory representations might underlie this convergence. Drawing on a recent distinction between object- and spatially-based visual imagery, we propose a putative model in which LOtv, a subregion of LOC, contains a modality-independent representation of geometric shape that can be accessed either bottom-up from direct sensory inputs or top-down from frontoparietal regions. We suggest that such access is modulated by object familiarity: spatial imagery may be more important for unfamiliar objects and involve IPS foci in facilitating somatosensory inputs to the LOC; by contrast, object imagery may be more critical for familiar objects, being reflected in prefrontal drive to the LOC.     

Representation of shapes, edges, and surfaces across multiple cues in the human visual cortex

The lateral occipital complex (LOC) responds preferentially to objects compared with random stimuli or textures independent of the visual cue. However, it is unknown whether the LOC (or other cortical regions) are involved in the processing of edges or global surfaces without shape information. Here, we examined processing of 1) global shape, 2) disconnected edges without a global shape, and 3) global surfaces without edges versus random stimuli across motion and stereo cues. The LOC responded more strongly to global shapes than to edges, surfaces, or random stimuli, for both motion and stereo cues. However, its responses to local edges or global surfaces were not different from random stimuli. This suggests that the LOC processes shapes, not edges or surfaces. LOC also responded more strongly to objects than to holes with the same shape, suggesting sensitivity to border ownership. V7 responded more strongly to edges than to surfaces or random stimuli for both motion and stereo cues, whereas V3a and V4 preferred motion edges. Finally, a region in the caudal intraparietal sulcus (cIPS) responded more strongly to both stereo versus motion and to stereo surfaces versus random stereo (but not to motion surfaces vs. random motion). Thus we found evidence for cue-specific responses to surfaces in the cIPS, both cue-specific and cue-independent responses to edges in intermediate visual areas, and shape-selective responses across multiple cues in the LOC. Overall, these data suggest that integration of visual information across multiple cues is mainly achieved at the level of shape and underscore LOC's role in shape computations.     

Object-selective responses in the human motion area MT/MST.

The perception of moving objects and our successful interaction with them entail that the visual system integrates shape and motion information about objects. However, neuroimaging studies have implicated different human brain regions in the analysis of visual motion (medial temporal cortex; MT/MST) and shape (lateral occipital complex; LOC), consistent with traditional approaches in visual processing that attribute shape and motion processing to anatomically and functionally separable neural mechanisms. Here we demonstrate object-selective fMRI responses (higher responses for intact than for scrambled images of objects) in MT/MST, and especially in a ventral subregion of MT/MST, suggesting that human brain regions involved mainly in the processing of visual motion are also engaged in the analysis of object shape.     

Metamers of the ventral stream

The human capacity to recognize complex visual patterns emerges in a sequence of brain areas known as the ventral stream, beginning with primary visual cortex (V1). We developed a population model for mid-ventral processing, in which nonlinear combinations of V1 responses are averaged in receptive fields that grow with eccentricity. To test the model, we generated novel forms of visual metamers, stimuli that differ physically but look the same. We developed a behavioral protocol that uses metameric stimuli to estimate the receptive field sizes in which the model features are represented. Because receptive field sizes change along the ventral stream, our behavioral results can identify the visual area corresponding to the representation. Measurements in human observers implicate visual area V2, providing a new functional account of neurons in this area. The model also explains deficits of peripheral vision known as crowding, and provides a quantitative framework for assessing the capabilities and limitations of everyday vision.     

Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry

During binocular rivalry, two incompatible monocular images compete for perceptual dominance, with one pattern temporarily suppressed from conscious awareness. We measured fMRI signals in early visual cortex while subjects viewed rival dichoptic images of two different contrasts; the contrast difference served as a 'tag' for the neuronal representations of the two monocular images. Activity in primary visual cortex (V1) increased when subjects perceived the higher contrast pattern and decreased when subjects perceived the lower contrast pattern. These fluctuations in V1 activity during rivalry were about 55% as large as those evoked by alternately presenting the two monocular images without rivalry. The rivalry-related fluctuations in V1 activity were roughly equal to those observed in other visual areas (V2, V3, V3a and V4v). These results challenge the view that the neuronal mechanisms responsible for binocular rivalry occur primarily in later visual areas.     

Privileged coding of convex shapes in human object-selective cortex

What is the neural code for object shape? Despite intensive research, the precise nature of object representations in high-level visual cortex remains elusive. Here we use functional magnetic resonance imaging (fMRI) to show that convex shapes are encoded in a privileged fashion by human lateral occipital complex (LOC), a region that has been implicated in object recognition. On each trial, two convex or two concave shapes that were either identical or different were presented sequentially. Critically, the convex and concave stimuli were the same except for a binocular disparity change that reversed the figure-ground assignment. The fMRI response in LOC for convex stimuli was higher for different than that for identical shape pairs, indicating sensitivity to differences in convex shape. However, when the same stimuli were seen as concave, the response for different and identical pairs was the same, indicating lower sensitivity to changes in concave shape than convex shape. This pattern was more pronounced in the anterior than that in the posterior portion of LOC. These results suggest that convex contours could be important elements in cortical object representations.