What Is Actually Affected by the Scrambling of Objects When Localizing the Lateral Occipital Complex?

The lateral occipital complex (LOC), the cortical region critical for shape perception, is localized with fMRI by its greater BOLD activity when viewing intact objects compared with their scrambled versions (resembling texture). Despite hundreds of studies investigating LOC, what the LOC localizer accomplishes-beyond distinguishing shape from texture-has never been resolved. By independently scattering the intact parts of objects, the axis structure defining the relations between parts was no longer defined. This led to a diminished BOLD response, despite the increase in the number of independent entities (the parts) produced by the scattering, thus indicating that LOC specifies interpart relations, in addition to specifying the shape of the parts themselves. LOC's sensitivity to relations is not confined to those between parts but is also readily apparent between objects, rendering it-and not subsequent "place" areas-as the critical region for the representation of scenes. Moreover, that these effects are witnessed with novel as well as familiar intact objects and scenes suggests that the relations are computed on the fly, rather than being retrieved from memory.

Ha ha! versus aha! a direct comparison of humor to nonhumorous insight for determining the neural correlates of mirth.

While humor typically involves a surprising discovery, not all discoveries are perceived as humorous or lead to a feeling of mirth. Is there a difference in the neural signature of humorous versus nonhumorous discovery? Subjects viewed drawings that were uninterpretable until a caption was presented that provided either: 1) a nonhumorous interpretation (or insight) of an object from an unusual or partial view (UV) or 2) a humorous interpretation (HU) of the image achieved by linking remote and unexpected concepts. fMRI activation elicited by the UV captions was a subset of that elicited by the humorous HU captions, with only the latter showing activity in the temporal poles and temporo-occipital junction (linking remote concepts), and medial prefrontal cortex (unexpected reward). Mirth may be a consequence of the linking of remote ideas producing high-and unexpected-activation in association and classical reward areas. We suggest that this process is mediated by opioid activity as part of a system rewarding attention to novel information.

Effective signaling of surface boundaries by L-vertices reflect the consistency of their contrast in natural images.

An L-vertex, the point at which two contours coterminate, provides highly reliable evidence that a surface terminates at that vertex, thus providing the strongest constraint on the extraction of shape from images (Guzman, 1968). Such vertices are pervasive in our visual world but the importance of a statistical regularity about them has been underappreciated: The contours defining the vertex are (almost) always of the same direction of contrast with respect to the background (i.e., both darker or both lighter). Here we show that when the two contours are of different directions of contrast, the capacity of the L-vertex to signal the termination of a surface, as reflected in object recognition, is markedly reduced. Although image statistics have been implicated in determining the connectivity in the earliest cortical visual stage (V1) and in grouping during visual search, this finding provides evidence that such statistics are involved in later stages where object representations are derived from two-dimensional images.

The Lateral Occipital Complex shows no net response to object familiarity.

In 1995, Malach et al. discovered an area whose fMRI BOLD response was greater when viewing intact, familiar objects than when viewing their scrambled versions (resembling texture). Since then hundreds of studies have explored this late visual region termed the Lateral Occipital Complex (LOC), which is now known to be critical for shape perception (James, Culham, Humphrey, Milner, & Goodale, 2003). Malach et al. (1995) discounted a role of familiarity by showing that "abstract" Henry Moore sculptures, unfamiliar to the subjects, also activated this region. This characterization of LOC as a region that responds to shape independently of familiarity has been accepted but never tested with control of the same low-level features. We assessed LOC's response to objects that had identical parts in two different arrangements, one familiar and the other novel. Malach was correct: There is no net effect of familiarity in LOC. However, a multivoxel correlation analysis showed that LOC does distinguish familiar from novel objects.

Neural correlates of face detection.

Although face detection likely played an essential adaptive role in our evolutionary past and in contemporary social interactions, there have been few rigorous studies investigating its neural correlates. MJH, a prosopagnosic with bilateral lesions to the ventral temporal-occipital cortices encompassing the posterior face areas (fusiform and occipital face areas), expresses no subjective difficulty in face detection, suggesting that these posterior face areas do not mediate face detection exclusively. Despite his normal contrast sensitivity and visual acuity in foveal vision, the present study nevertheless revealed significant face detection deficits in MJH. Compared with controls, MJH showed a lower tolerance to noise in the phase spectrum for faces (vs. cars), reflected in his higher detection threshold for faces. MJH's lesions in bilateral occipito-temporal cortices thus appear to have produced a deficit not only in face individuation, but also in face detection.

Using the reassignment procedure to test object representation in pigeons and people.

In four experiments, we evaluated Lea's (1984) reassignment procedure for studying object representation in pigeons (Experiments 1-3) and humans (Experiment 4). In the initial phase of Experiment 1, pigeons were taught to make discriminative button responses to five views of each of four objects. Using the same set of buttons in the second phase, one view of each object was trained to a different button. In the final phase, the four views that had been withheld in the second stage were shown. In Experiment 2, pigeons were initially trained just like the birds in Experiment 1. Then, one view of each object was reassigned to a different button, now using a new set of four response buttons. In Experiment 3, the reassignment paradigm was again tested using the number of pecks to bind together different views of the same object. Across all three experiments, pigeons showed statistically significant generalization of the new response to the non-reassigned views, but such responding was well below that to the reassigned view. In Experiment 4, human participants were studied using the same stimuli and task as the pigeons in Experiment 1. People did strongly generalize the new response to the non-reassigned views. These results indicate that humans, but not pigeons, can employ a unified object representation that they can flexibly map to different responses under the reassignment procedure.

Cortical representation of medial axis structure.

The identity of an object is not only specified by its parts but also by the relations among the parts. Rearranging parts can produce a completely different object, in the same manner as rearranging the phonemes in "fur" can yield "rough." How does the visual system represent the relative positions of parts? Between-part relations can be characterized by specifying the relations between the medial axes (imaginary lines through the centers) of an object's parts. A functional magnetic resonance imaging multivoxel classification study tested whether the medial axis structure is represented in the human visual system independent of part identity and overall object orientation. Stimuli were line drawings of novel 3-part geometrical objects, which differed in the relations between their parts' medial axes (i.e., in their medial axis structures), the geons that composed each object, and the objects' orientations in plane and in depth. In regions of interest throughout visual cortex, a support vector machine classifier was trained to distinguish objects that shared either the same medial axis structures or the same orientations. By the level of V3, different medial axis structures were more accurately classified than different orientations, indicating a change in the representation of shape compared with earlier visual areas.

A neurocomputational account of the face configural effect.

A striking phenomenon in face perception is the configural effect in which a difference in a single part appears more distinct in the context of a face than it does by itself. The face context would be expected to increase search complexity, rendering discrimination more--not less--difficult. Remarkably, there has never been a biologically plausible explanation of this fundamental signature of face recognition.We show that the configural effect can be simply derived from a model composed of overlapping receptive fields (RFs) characteristic of early cortical simple-cell tuning but also present in face-selective areas. Because of the overlap in RFs, the difference in a single part is not only represented in the RFs centered on it but also propagated to larger RFs centered on distant parts of the face. Dissimilarity values computed from the model between pairs of faces and pairs of face parts closely matched the recognition accuracy of human observers who had learned a set of faces composed of composite parts and were tested on wholes (Which is Larry?) and parts (Which is Larry's nose?). When stimuli were high versus low passed the contributions of different spatial frequency (SF) bands to the configural effect were largely comparable. Therefore, it was the larger RFs rather than the low SFs that accounted for most of the configural effect. The representation explains why, relative to objects, face recognition is so adversely affected by inversion and contrast reversal and why distinctions between similar faces are ineffable.

The benefit of object interactions arises in the lateral occipital cortex independent of attentional modulation from the intraparietal sulcus: a transcranial magnetic stimulation study.

Our visual experience is generally not of isolated objects, but of scenes, where multiple objects are interacting. Such interactions (e.g., a watering can positioned to pour water toward a plant) have been shown to facilitate object identification compared with when the objects are depicted as not interacting (e.g., a watering can positioned away from the plant) (Green and Hummel, 2004, 2006). What is the neural basis for this advantage? Recent fMRI studies have identified the lateral occipital cortex (LO) as a potential neural origin of this behavioral benefit, as LO showed greater responses to object pairs depicted as interacting compared with when they are not (Kim and Biederman, 2010; Roberts and Humphreys, 2010). However, it is possible that LO was modulated by an attention-sensitive region, the intraparietal sulcus (IPS), which sometimes showed a similar pattern of responses as that of LO in the Kim and Biederman (2010) investigation. To test this hypothesis, we delivered transcranial magnetic stimulation (TMS) to human subjects' LO and IPS while they detected a target object that was or was not interacting with another object to form a scene. TMS delivered to LO but not IPS abolished the facilitation in identifying interacting objects compared with noninteracting depictions observed in the absence of TMS, suggesting that it is LO and not IPS that is critical for the coding of object interactions.

Greater sensitivity to nonaccidental than metric changes in the relations between simple shapes in the lateral occipital cortex.

Behavioral studies and single cell recordings in monkey inferotemporal cortex have documented greater sensitivity to differences in viewpoint invariant or nonaccidental properties (e.g., straight vs. curved), than metric properties (e.g., degree of curvature) of simple shapes. Are we similarly more sensitive to nonaccidental (NAP) than metric (MP) differences of the relations between objects? We addressed this question with sets of scene triplets that could, from a reference or "Base" scene (e.g., a brick slightly separated from a cylinder), undergo a NAP relational change (e.g., the brick attached to the cylinder) or an MP relational change (e.g., the brick further separated from the cylinder). Critically, both relational variations were matched in physical dissimilarity using pixel energy and the Gabor-jet system, a model of V1 similarity. In an adaptive staircase match-to-sample paradigm, subjects required more than double the presentation durations for detecting differences in MP than NAP relations to achieve equivalent levels of accuracy. In two fMRI experiments, NAP changes consistently produced greater responses in the lateral occipital cortex (LO), but not in earlier retinotopic stages, compared to MP changes, implicating LO as the potential neural locus for where the greater detectability of the differences of NAPs than MPs is made explicit. HMAX, a model of cell tuning in higher-level ventral visual areas, did not consistently reflect the marked NAP advantage witnessed in behavioral performance and in LO responses.

Where do objects become scenes?

Regions tuned to individual visual categories, such as faces and objects, have been discovered in the later stages of the ventral visual pathway in the cortex. But most visual experience is composed of scenes, where multiple objects are interacting. Such interactions are readily described by prepositions or verb forms, for example, a bird perched on a birdhouse. At what stage in the pathway does sensitivity to such interactions arise? Here we report that object pairs shown as interacting, compared with their side-by-side depiction (e.g., a bird besides a birdhouse), elicit greater activity in the lateral occipital complex, the earliest cortical region where shape is distinguished from texture. Novelty of the interactions magnified this gain, an effect that was absent in the side-by-side depictions. Scene-like relations are thus likely achieved simultaneously with the specification of object shape.

The sizable difficulty in matching unfamiliar faces differing only moderately in orientation in depth is a function of image dissimilarity.

Attempting to match unfamiliar, highly similar faces at moderate differences in orientation in depth is surprisingly difficult. No neurocomputational account of these costs that addressed the representation of faces by which a face-similarity metric can be derived has been offered. A metric specifying the similarity of the to-be-distinguished faces is required as the rotation costs will be a function of the difficulty in distinguishing the faces. Consequently, rotation costs have typically been described in terms of angle of disparity, rather than the dissimilarity of the faces produced by the rotation. We assessed the effects of orientation disparity in a match-to-sample paradigm of a simultaneous presentation of a triangular display of three faces. Two lower test faces, a matching face and a foil, were always at the same orientation and differed by 0° to 20° from the sample on top. The similarity of the images was scaled by a model based on simple cell tuning, modeled as Gabor wavelets, that correlates almost perfectly with psychophysical similarity. Two measures of face similarity, with approximately additive effects on reaction times, accounted for matching performance: a) the decrease in similarity between the images of the matching and sample faces produced by increases in their orientation disparity, and b) the similarity between the matching face and the selection of a particular foil. The 20° orientation disparity was sufficient to yield a sizeable 301 msec increase in reaction time. An implication of the results is that the activity in V1 produced by viewing a face is fed forward to areas responsible for the individuation of that face.

Loci of the release from fMRI adaptation for changes in facial expression, identity, and viewpoint.

Face recognition involves collaboration of a distributed network of neural correlates. However, how different attributes of faces are represented has remained unclear. We used functional magnetic resonance imaging-adaptation (fMRIa) to investigate the representation of viewpoint, expression, and identity of faces in the fusiform face area (FFA) and the occipital face area (OFA). In an event-related experiment, subjects viewed sequences of two faces and judged whether they depicted the same person. The images could vary in viewpoint, expression and/or identity. Critically, the physical similarity between view-changed and between expression-changed faces of the same person were matched by the Gabor-jet metric, a measure that predicts almost perfectly the effects of image similarity on face discrimination performance. In FFA, changes of identity produced the largest release from adaptation followed by changes of expression; but the release caused by changes of viewpoint was smaller and not reliable. OFA was sensitive only to changes in identity, even when image changes produced by identity variations were matched to those of expression and orientation. These results suggest that FFA is involved in the perception of both identity and expression of faces, a result contrary to the hypothesis of independent processing of changeable and invariant attributes of faces in the face-processing network.

Vision: A Product of a Society of Independent Experts.

A lesion of primary visual cortex, V1, can result in the perceived size of objects varying with the size of their retinal image. A new study shows that the pregrasp span of the hand of an individual with such a lesion remains tuned to the object's true size, providing evidence for separate representations mediating perceptual appearance and motor interactions.

Visual noise consisting of X-junctions has only a minimal adverse effect on object recognition.

In 1968, Guzman showed that the myriad of surfaces composing a highly complex and novel assemblage of volumes can readily be assigned to their appropriate volumes in terms of the constraints offered by the vertices of coterminating edges. Of particular importance was the L-vertex, produced by the cotermination of two contours, which provides strong evidence for the termination of a 2-D surface. An X-junction, formed by the crossing of two contours without a change of direction at the crossing, played no role in the segmentation of a scene. If the potency of noise elements to affect recognition performance reflects their relevancy to the segmentation of scenes, as was suggested by Guzman, gaps in an object's contours bounded by irrelevant X-junctions would be expected to have little or no adverse effect on shape-based object recognition, whereas gaps bounded by L-junctions would be expected to have a strong deleterious effect when they disrupt the smooth continuation of contours. Guzman's roles for the various vertices and junctions have never been put to systematic test with respect to human object recognition. By adding identical noise contours to line drawings of objects that produced either L-vertices or X-junctions, these shape features could be compared with respect to their disruption of object recognition. Guzman's insights that irrelevant L-vertices should be highly disruptive and irrelevant X-vertices would have only a minimal deleterious effect were confirmed.

Representation of shape in individuals from a culture with minimal exposure to regular, simple artifacts: sensitivity to nonaccidental versus metric properties.

Many of the phenomena underlying shape recognition can be derived from the greater sensitivity to nonaccidental properties of an image (e.g., whether a contour is straight or curved), which are invariant to orientation in depth, than to the metric properties of an image (e.g., a contour's degree of curvature), which can vary with orientation. What enables this sensitivity? One explanation is that it derives from people's immersion in a manufactured world in which simple, regular shapes distinguished by nonaccidental properties abound (e.g., a can, a brick), and toddlers are encouraged to play with toy shape sorters. This report provides evidence against this explanation. The Himba, a seminomadic people living in a remote region of northwestern Namibia where there is little exposure to regular, simple artifacts, were virtually identical to Western observers in their greater sensitivity to nonaccidental properties than to metric properties of simple shapes.

A face in a (temporal) crowd.

Familiar objects, specified by name, can be identified with high accuracy when embedded in a rapidly presented sequence of images at rates exceeding 10 images/s. Not only can target objects be detected at such brief presentation rates, they can also be detected under high uncertainty, where their classification is defined negatively, e.g., "Not a Tool." The identification of a familiar speaker's voice declines precipitously when uncertainty is increased from one to a mere handful of possible speakers. Is the limitation imposed by uncertainty, i.e., the number of possible individuals, a general characteristic of processes for person individuation such that the identifiability of a familiar face would undergo a similar decline with uncertainty? Specifically, could the presence of an unnamed celebrity, thus any celebrity, be detected when presented in a rapid sequence of unfamiliar faces? If so, could the celebrity be identified? Despite the markedly greater physical similarity of faces compared to objects that are, say, not tools, the presence of a celebrity could be detected with moderately high accuracy (∼75%) at rates exceeding 7 faces/s. False alarms were exceedingly rare as almost all the errors were misses. Detection accuracy by moderate congenital prosopagnosics was lower than controls, but still well above chance. Given the detection of the presence of a celebrity, all subjects were almost always able to identify that celebrity, providing no role for a covert familiarity signal outside of awareness.

Pigeons spontaneously form three-dimensional shape categories.

We explored the pigeon's representation of the shape of simple three-dimensional objects (geons) rotated in depth (four views each of four geons). Pigeons assigned to the Categorization group had to respond differentially to images of four different geons-termed arch, barrel, brick, and wedge-based on their 3D shape, regardless of the orientation of the object. Pigeons assigned to the Pseudocategorization group had to respond differentially to the same objects based on groupings that did not correspond to object identity, which required the learning of local orientation-dependent features (e.g., a concave curve on top, or the position of an illumination hotspot). The Categorization group, which could employ object-identity representations, quickly achieved highly accurate responding. The Pseudocategorization group, however, failed to achieve reliable above-chance responding. In addition, the reaction times for the Categorization group were significantly shorter than for the Pseudocategorization group. These results indicate that pigeons show a strong, spontaneous tendency to categorize the shapes of different orientations in depth of the same 3D object as similar, if not equivalent; they do so despite the vast differences in image characteristics caused by the variations in orientations, even when such categorization is contrary to the reinforcement contingencies.

Pigeons and humans are more sensitive to nonaccidental than to metric changes in visual objects.

Humans and macaques are more sensitive to differences in nonaccidental image properties, such as straight vs. curved contours, than to differences in metric properties, such as degree of curvature [Biederman, I., Bar, M., 1999. One-shot viewpoint invariance in matching novel objects. Vis. Res. 39, 2885-2899; Kayaert, G., Biederman, I., Vogels, R., 2003. Shape tuning in macaque inferior temporal cortex. J. Neurosci. 23, 3016-3027; Kayaert, G., Biederman, I., Vogels, R., 2005. Representation of regular and irregular shapes in macaque inferotemporal cortex. Cereb. Cortex 15, 1308-1321]. This differential sensitivity allows facile recognition when the object is viewed at an orientation in depth not previously experienced. In Experiment 1, we trained pigeons to discriminate grayscale, shaded images of four shapes. Pigeons made more confusion errors to shapes that shared more nonaccidental properties. Although the images in that experiment were not well controlled for incidental changes in metric properties, the same results were apparent with better controlled stimuli in Experiment 2: pigeons trained to discriminate a target shape from a metrically changed shape and a nonaccidentally changed shape committed more confusion errors to the metrically changed shape, suggesting that they perceived it to be more similar to the target shape. Humans trained with similar stimuli and procedure exhibited the same tendency to make more errors to the metrically changed shape. These results document the greater saliency of nonaccidental differences for shape recognition and discrimination in a non-primate species and suggest that nonaccidental sensitivity may be characteristic of all shape-discriminating species.

The cognitive neuroscience of person identification.

We compare and contrast five differences between person identification by voice and face. 1. There is little or no cost when a familiar face is to be recognized from an unrestricted set of possible faces, even at Rapid Serial Visual Presentation (RSVP) rates, but the accuracy of familiar voice recognition declines precipitously when the set of possible speakers is increased from one to a mere handful. 2. Whereas deficits in face recognition are typically perceptual in origin, those with normal perception of voices can manifest severe deficits in their identification. 3. Congenital prosopagnosics (CPros) and congenital phonagnosics (CPhon) are generally unable to imagine familiar faces and voices, respectively. Only in CPros, however, is this deficit a manifestation of a general inability to form visual images of any kind. CPhons report no deficit in imaging non-voice sounds. 4. The prevalence of CPhons of 3.2% is somewhat higher than the reported prevalence of approximately 2.0% for CPros in the population. There is evidence that CPhon represents a distinct condition statistically and not just normal variation. 5. Face and voice recognition proficiency are uncorrelated rather than reflecting limitations of a general capacity for person individuation.