Human Lateral Occipital Complex Research Articles

Neuronal tuning and population representations of shape and category in human visual cortex

Object recognition and categorization are essential cognitive processes which engage considerable neural resources in the human ventral visual stream. However, the tuning properties of human ventral stream neurons for object shape and category are virtually unknown. We performed large-scale recordings of spiking activity in human Lateral Occipital Complex in response to stimuli in which the shape dimension was dissociated from the category dimension. Consistent with studies in nonhuman primates, the neuronal representations were primarily shape-based, although we also observed category-like encoding for images of animals. Surprisingly, linear decoders could reliably classify stimulus category even in data sets that were entirely shape-based. In addition, many recording sites showed an interaction between shape and category tuning. These results represent a detailed study on shape and category coding at the neuronal level in the human ventral visual stream, furnishing essential evidence that reconciles human imaging and macaque single-cell studies.

Single-cell selectivity and functional architecture of human lateral occipital complex.

The human lateral occipital complex (LOC) is more strongly activated by images of objects compared to scrambled controls, but detailed information at the neuronal level is currently lacking. We recorded with microelectrode arrays in the LOC of 2 patients and obtained highly selective single-unit, multi-unit, and high-gamma responses to images of objects. Contrary to predictions derived from functional imaging studies, all neuronal properties indicated that the posterior subsector of LOC we recorded from occupies an unexpectedly high position in the hierarchy of visual areas. Notably, the response latencies of LOC neurons were long, the shape selectivity was spatially clustered, LOC receptive fields (RFs) were large and bilateral, and a number of LOC neurons exhibited three-dimensional (3D)-structure selectivity (a preference for convex or concave stimuli), which are all properties typical of end-stage ventral stream areas. Thus, our results challenge prevailing ideas about the position of the more posterior subsector of LOC in the hierarchy of visual areas.

Non-holistic coding of objects in lateral occipital complex with and without attention

A fundamental issue in visual cognition is whether high-level visual areas code objects in a part-based or a view-based (holistic) format. Previous behavioral and neuroimaging studies that examined the viewpoint invariance of object recognition have yielded ambiguous results, providing evidence for either type of representational format. A critical factor distinguishing the two formats could be the availability of attentional resources, as a number of priming studies have found greater viewpoint invariance for attended compared to unattended objects. It has therefore been suggested that the activation of part-based representations requires attention, whereas the activation of holistic representations occurs automatically irrespective of attention. Using functional magnetic resonance imaging in combination with a novel multivariate pattern analysis approach, the present study probed the format of object representations in human lateral occipital complex and its dependence on attention. We presented human participants with intact and half-split versions of objects that were either attended or unattended. Cross-classifying between intact and split objects, we found that the object-related information coded in activation patterns of intact objects is fully preserved in the patterns of split objects and vice versa. Importantly, the generalization between intact and split objects did not depend on attention. We conclude that lateral occipital complex codes objects in a non-holistic format, both in the presence and absence of attention.

"What?" and "where?" versus "what is where?": The impact of task on coding of object form and position in the lateral occipital complex

Fast and accurate recognition of both the identities and positions of objects in visual space is critical to deciphering visual environments. Studies in both humans and nonhuman primates have demonstrated that neural populations in ventral temporal visual areas are jointly tuned to both the form and position of objects, allowing information about the identities of objects to be "tagged" with their positions. Because not all behaviors demand that the identities of objects be associated with position information with equal precision, however, the present study asked whether the spatial tuning of form-encoding populations in the human lateral occipital complex (LOC) is sculpted by task demands. Subjects were scanned using functional magnetic resonance imaging while viewing matches of the game Rock, Paper, Scissors played with exemplar pairs from those categories. Subjects first performed a repetition-detection task that depended on object form but not position; subsequently, subjects viewed the same stimuli while determining the position of each pair's "winner," a task that depended upon the conjunction of object form and position. Compared to data from the initial scan, multivoxel activity patterns evoked in the lateral occipital (LO) subdivision of LOC while subjects judged winners showed enhanced sensitivity to the relative positions of objects in pairs. Although superficially consistent with dynamic position tuning, this effect appears to be attributable to an accompanying task-dependent improvement in the sensitivity of LO populations to object form. The results thus suggest that the spatial tuning of form-encoding populations in LO does not depend upon the precision of spatial information demanded by a task.

Joint neuronal tuning for object form and position in the human lateral occipital complex

A long-standing heuristic in visual neuroscience holds that extrastriate visual cortex is parceled into a dorsal "where" pathway concerned with stimulus position and motion and a ventral "what" pathway concerned with stimulus form. Several recent studies using functional magnetic resonance imaging (fMRI), however, have shown that small changes in the position of a single object can produce reliable changes in activity patterns in object-selective lateral occipital complex (LOC). Although these data demonstrate that information about both object form and position is present at the region level in LOC, the extent to which they reflect joint neuronal tuning to these dimensions is unclear. To measure joint tuning for form and position, we used fMRI to record patterns of activity evoked in LOC and other visual areas while subjects viewed pairs of objects that varied in category content, overall position, and relative object position. Consistent with previous results, multivoxel activity patterns in LOC varied reliably with the category content and position of object pairs. Moreover, activity patterns in the lateral occipital (LO) subregion of LOC varied significantly with the relative positions of objects within pairs, even when absolute pair position was constant. This result provides strong evidence for the existence of neuronal populations in LO which are jointly tuned for both object form (i.e., category) and position.

Encoding the identity and location of objects in human LOC

We are able to recognize objects independent of their location in the visual field. At the same time, we also keep track of the location of objects to orient ourselves and to interact with the environment. The lateral occipital complex (LOC) has been suggested as the prime cortical region for representation of object identity. However, the extent to which LOC also represents object location has remained debated. In this study we used high-resolution fMRI in combination with multivoxel pattern classification to investigate the cortical encoding of three object exemplars from four different categories presented in two different locations. This approach allowed us to study location-tolerant object information and object-tolerant location information in LOC, both at the level of categories and exemplars. We found evidence for both location-tolerant object information and object-tolerant location information in LOC at the level of categories and exemplars. Our results further highlight the mixing of identity and location information in the ventral visual pathway.

Processing of perceived shape vs. contours in the human lateral occipital complex

Processing of perceived shape vs. contours in the human lateral occipital complex

FMRI responses to perceptually completed regions in the human lateral occipital complex: Bounding illusory contours are not a necessary condition

fMRI responses to perceptually completed regions in the human lateral occipital complex: Bounding illusory contours are not a necessary condition

Tactile shape discrimination recruits human lateral occipital complex during early perceptual processing

Neuroimaging studies investigating somatosensory-based object recognition in humans have revealed activity in the lateral occipital complex, a cluster of regions primarily associated with visual object recognition. To date, determining whether this activity occurs during or subsequent to recognition per se, has been difficult to assess due to the low temporal resolution of the hemodynamic response. To more finely measure the timing of somatosensory object recognition processes we employed high density EEG using a modified version of a paradigm previously applied to neuroimaging experiments. Simple geometric shapes were presented to the right index finger of 10 participants while the ongoing EEG was measured time locked to the stimulus. In the condition of primary interest participants discriminated the shape of the stimulus. In the alternate condition they judged stimulus duration. Using traditional event-related potential analysis techniques we found significantly greater amplitudes in the evoked potentials of the shape discrimination condition between 140 and 160 ms, a timeframe in which LOC mediated perceptual processes are believed to occur during visual object recognition. Scalp voltage topography and source analysis procedures indicated the lateral occipital complex as the likely source behind this effect. This finding supports a multisensory role for the lateral occipital complex during object recognition.

Early processing in the human lateral occipital complex is highly responsive to illusory contours but not to salient regions

Human electrophysiological studies support a model whereby sensitivity to so-called illusory contour stimuli is first seen within the lateral occipital complex. A challenge to this model posits that the lateral occipital complex is a general site for crude region-based segmentation, based on findings of equivalent hemodynamic activations in the lateral occipital complex to illusory contour and so-called salient region stimuli, a stimulus class that lacks the classic bounding contours of illusory contours. Using high-density electrical mapping of visual evoked potentials, we show that early lateral occipital cortex activity is substantially stronger to illusory contour than to salient region stimuli, whereas later lateral occipital complex activity is stronger to salient region than to illusory contour stimuli. Our results suggest that equivalent hemodynamic activity to illusory contour and salient region stimuli probably reflects temporally integrated responses, a result of the poor temporal resolution of hemodynamic imaging. The temporal precision of visual evoked potentials is critical for establishing viable models of completion processes and visual scene analysis. We propose that crude spatial segmentation analyses, which are insensitive to illusory contours, occur first within dorsal visual regions, not the lateral occipital complex, and that initial illusory contour sensitivity is a function of the lateral occipital complex.

Attention-Dependent Representation of a Size Illusion in Human V1

One of the most fundamental properties of human primary visual cortex (V1) is its retinotopic organization, which makes it an ideal candidate for encoding spatial properties, such as size, of objects. However, three-dimensional (3D) contextual information can lead to size illusions that are reflected in the spatial pattern of activity in V1 [1]. A critical question is how complex 3D contextual information can influence spatial activity patterns in V1. Here, we assessed whether changes in the spatial distribution of activity in V1 depend on the focus of attention, which would be suggestive of feedback of 3D contextual information from higher visual areas. We presented two 3D rings at close and far apparent depths in a 3D scene. When subjects fixated its center, the far ring appeared to be larger and occupy a more eccentric portion of the visual field, relative to the close ring. Using functional magnetic resonance imaging, we found that the spatial distribution of V1 activity induced by the far ring was also shifted toward a more eccentric representation of the visual field, whereas that induced by the close ring was shifted toward the foveal representation, consistent with their perceptual appearances. This effect was significantly reduced when the focus of spatial attention was narrowed with a demanding central fixation task. We reason that focusing attention on the fixation task resulted in reduced activity in--and therefore reduced feedback from--higher visual areas that process the 3D depth cues.

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.

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.

FMRI Activity Patterns in Human LOC Carry Information about Object Exemplars within Category

Abstract The lateral occipital complex (LOC) is a set of areas in the human occipito-temporal cortex responding to objects as opposed to low-level control stimuli. Conventional functional magnetic resonance imaging (fMRI) analysis methods based on regional averages could not detect signals discriminative of different types of objects in this region. Here, we examined fMRI signals using multivariate pattern recognition (support vector classification) to systematically explore the nature of object-related information available in fine-grained activity patterns in the LOC. Distributed fMRI signals from the LOC allowed for above-chance discrimination not only of the category but also of within-category exemplars of everyday man-made objects, and such exemplar-specific information generalized across changes in stimulus size and viewpoint, particularly in posterior subregions. Object identity could also be predicted from responses of the early visual cortex, even significantly across the changes in size and viewpoint used here. However, a dissociation was observed between these two regions of interest in the degree of discrimination for objects relative to size: In the early visual cortex, two different sizes of the same object were even better discriminated than two different objects (in accordance with measures of pixelwise stimulus similarity), whereas the opposite was true in the LOC. These findings provide the first evidence that direct evoked fMRI activity patterns in the LOC can be different for individual object exemplars (within a single category). We propose that pattern recognition methods as used here may provide an alternative approach to study mechanisms of neuronal representation based on aspects of the fMRI response independent of those assessed in adaptation paradigms.

FMRI activity patterns in human LOC carry information about object exemplars within category.

Abstract The lateral occipital complex (LOC) is a set of areas in the human occipito-temporal cortex responding to objects as opposed to low-level control stimuli. Conventional functional magnetic resonance imaging (fMRI) analysis methods based on regional averages could not detect signals discriminative of different types of objects in this region. Here, we examined fMRI signals using multivariate pattern recognition (support vector classification) to systematically explore the nature of object-related information available in fine-grained activity patterns in the LOC. Distributed fMRI signals from the LOC allowed for above-chance discrimination not only of the category but also of within-category exemplars of everyday man-made objects, and such exemplar-specific information generalized across changes in stimulus size and viewpoint, particularly in posterior subregions. Object identity could also be predicted from responses of the early visual cortex, even significantly across the changes in size and viewpoint used here. However, a dissociation was observed between these two regions of interest in the degree of discrimination for objects relative to size: In the early visual cortex, two different sizes of the same object were even better discriminated than two different objects (in accordance with measures of pixelwise stimulus similarity), whereas the opposite was true in the LOC. These findings provide the first evidence that direct evoked fMRI activity patterns in the LOC can be different for individual object exemplars (within a single category). We propose that pattern recognition methods as used here may provide an alternative approach to study mechanisms of neuronal representation based on aspects of the fMRI response independent of those assessed in adaptation paradigms.

Beyond Retinotopic Mapping: The Spatial Representation of Objects in the Human Lateral Occipital Complex

The spatial representation in the human ventral object-related areas (i.e., the lateral occipital complex [LOC]) is currently unknown. It seems plausible, however, that it would diverge from the strict retinotopic mapping (characteristic of V1) to a more invariant coordinate frame, thereby allowing for reliable object recognition in the face of eye, head, or body movement. To study this, we compared the fMRI activation in LOC when object displacement was limited to either the retina or the screen by manipulating eye position and object locations. We found clear adaptation in LOC when the object's screen position was fixed, regardless of the object's retinal position. Furthermore, we found significantly greater activation in LOC in the hemisphere contralateral to the object's screen position, although the visual task was constructed in a way that the objects were present equally often on each of the 2 retinal hemifields. Together, these results indicate that a sizeable fraction of the neurons in LOC may have head-based receptive fields. Such an extraretinal representation may be useful for maintenance of object coherence across saccadic eye movements, which are an integral part of natural vision.

Activation time course of responses to illusory contours and salient region: A high-density electrical mapping comparison

Until recently, early visual areas (V1/V2) were believed to respond mainly to illusory contours (ICs). At present, however, functional neuroimaging suggests that the human lateral occipital complex (LOC), a higher tier than V2, responds strongly to ICs and that IC-related activation in V1/V2 in fact might be driven by feedback input from the LOC. When Kanizsa-type ICs are modified by rounding the corners of the inducers and misaligning them slightly, the impression of an enclosed salient region (SR) remains, although ICs no longer are perceived. Stanley and Rubin (Stanley, D.A., Rubin, N., 2003. fMRI activation in response to illusory contours and salient regions in the human lateral occipital complex. Neuron, 37, 323–331) found that the LOC responded to SR, suggesting that the LOC subserves a rapid but crude region-based segmentation process preceding boundary completion in V1/V2. The present study compared the time course of cortical responses to ICs with those to SR using high-density (74-channel) event-related potentials (ERPs). Scalp mapping and statistical analysis indicated that shared negative modulation for ICs and SR was distributed bilaterally over the lateral occipital scalp at a latency of 70 to 180 ms. Slightly later, a weak negative modulation occurred with ICs but not SR at the occipital pole scalp from 170 to 180 ms. Dipoles for early and late modulations were fitted optimally in the LOC and occipital pole, respectively. The present results suggested that IC-related cortical activation could be separated into region-based segmentation and subsequent boundary completion.

Object and shape processing in the human lateral occipital complex

Object and shape processing in the human lateral occipital complex

Greater sensitivity to convexities than concavities in human lateral occipital complex

Greater sensitivity to convexities than concavities in human lateral occipital complex

Using Functional Magnetic Resonance Imaging to Assess Adaptation and Size Invariance of Shape Processing by Humans and Monkeys

Functional magnetic resonance imaging in awake monkeys and humans was used to compare object adaptation in shape-sensitive regions of these two species under identical and different size conditions. Object adaptation was similar in humans and monkeys under both conditions. Neither species showed complete size invariance, in agreement with single-cell studies. Both the macaque inferotemporal (IT) complex and human lateral occipital complex (LOC) displayed an anteroposterior gradient in object adaptation and size invariance, with the more anterior regions being more adaptable and size invariant. The results provide additional evidence for the homology between the macaque IT cortex and human LOC but also add to the growing list of differences between human and monkey intraparietal sulcus regions.