In primates, the presence of a face in a visual scene captures attention and rapidly directs the observer's gaze to the face, even when the face is not relevant to the task at hand. Here, we explored a neural circuit that might potentially play a causal role in this powerful behavior. In our previous research, two monkeys received microinfusions of muscimol, a GABAA-receptor agonist, or saline (as a control condition) in separate sessions into individual or pairs of four inferotemporal face patches (middle and anterior lateral and fundal), as identified by a preceding face localizer experiment. Then, using fMRI, we measured the impact of each inactivation condition on responses in the other face patches relative to the control condition. In this study, we used the same method and measured the impact of each inactivation condition on responses in the FEF and the lateral intraparietal area, two regions associated with attentional processing, while face and nonface object stimuli were viewed. Our results revealed potential relationships between inferotemporal face patches and these two attention-related regions: The inactivation of the middle lateral and anterior fundal face patches had a pronounced impact on FEF, whereas the inactivation of the middle and anterior lateral face patches might have a noticeable influence on lateral intraparietal area. Together, these initial exploratory findings document a circuit that potentially underlies the attentional capture of faces. Confirmation of the role of this circuit remains to be accomplished in the context of paradigm explicitly testing the attentional capture of faces.

Despite our differences, there is much about the natural visual world that most observers perceive in common. Across adults, approximately 30% of the brain is activated in a consistent fashion while viewing naturalistic input. At what stage of development is this consistency of neural profile across individuals present? Here, we focused specifically on whether this mature profile is present in adolescence, a key developmental period that bridges childhood and adulthood, and in which new cognitive and social challenges are at play. We acquired fMRI data evoked by a movie shown twice to younger (9–14 years old) and older adolescents (15–19 years old) and to adults, and conducted three key analyses. First, we characterized the consistency of the neural response within individuals (across separate runs of the movie), then within individuals of the same age group, and, last, between age groups. The neural consistency within individuals was similar across age groups with reliable activation in largely overlapping but slightly different cortical regions. In contrast, somewhat differing regions exhibited higher within-age correlations in both groups of adolescents than in the adults. Last, across the whole cortex, we identified regions evincing different patterns of maturation across age. Together, these findings provide a fine-grained characterization of functional neural development in adolescence and uncover signatures of widespread change in cortical coherence that supports the emerging mature stereotypical responses to naturalistic stimuli. These results also offer a more nuanced account of development that obeys neither a rigid linear progression nor a large qualitative change over time.

Studies of the emergence of shape representations in childhood have focused primarily on the ventral visual pathway. Importantly, however, there is increasing evidence that, in adults, the dorsal pathway also represents shape-based information. These dorsal representations follow a gradient with more posterior regions being more shape-sensitive than anterior regions and with representational similarity in some posterior regions that is equivalent to that observed in some ventral regions. To explore the emergence and nature of dorsal shape representations in development, we acquired both fMRI BOLD signals and behavioral data in children (aged 8–10 years) using a parametric image scrambling paradigm. Children exhibited adult-like large-scale organization of shape processing along both ventral and dorsal pathways. Also, as in adults, the activation profiles of children's posterior dorsal and ventral regions were correlated with recognition performance, reflecting a possible contribution of these signals to perception. There were age-related changes, however, with children being more affected by the distortion of shape information than adults, both behaviorally and neurally. These findings reveal that shape-processing mechanisms along both dorsal and ventral pathways are subject to a protracted developmental trajectory.

Visual object recognition is performed effortlessly by humans notwithstanding the fact that it requires a series of complex computations, which are, as yet, not well understood. Here, we tested a novel account of the representations used for visual recognition and their neural correlates using fMRI. The rationale is based on previous research showing that a set of representations, termed “minimal recognizable configurations” (MIRCs), which are computationally derived and have unique psychophysical characteristics, serve as the building blocks of object recognition. We contrasted the BOLD responses elicited by MIRC images, derived from different categories (faces, objects, and places), sub-MIRCs, which are visually similar to MIRCs, but, instead, result in poor recognition and scrambled, unrecognizable images. Stimuli were presented in blocks, and participants indicated yes/no recognition for each image. We confirmed that MIRCs elicited higher recognition performance compared to sub-MIRCs for all three categories. Whereas fMRI activation in early visual cortex for both MIRCs and sub-MIRCs of each category did not differ from that elicited by scrambled images, high-level visual regions exhibited overall greater activation for MIRCs compared to sub-MIRCs or scrambled images. Moreover, MIRCs and sub-MIRCs from each category elicited enhanced activation in corresponding category-selective regions including fusiform face area and occipital face area (faces), lateral occipital cortex (objects), and parahippocampal place area and transverse occipital sulcus (places). These findings reveal the psychological and neural relevance of MIRCs and enable us to make progress in developing a more complete account of object recognition.

Although shape perception is primarily considered a function of the ventral visual pathway, previous research has shown that both dorsal and ventral pathways represent shape information. Here, we examine whether the shape-selective electrophysiological signals observed in dorsal cortex are a product of the connectivity to ventral cortex or are independently computed. We conducted multiple EEG studies in which we manipulated the input parameters of the stimuli so as to bias processing to either the dorsal or ventral visual pathway. Participants viewed displays of common objects with shape information parametrically degraded across five levels. We measured shape sensitivity by regressing the amplitude of the evoked signal against the degree of stimulus scrambling. Experiment 1, which included grayscale versions of the stimuli, served as a benchmark establishing the temporal pattern of shape processing during typical object perception. These stimuli evoked broad and sustained patterns of shape sensitivity beginning as early as 50 msec after stimulus onset. In Experiments 2 and 3, we calibrated the stimuli such that visual information was delivered primarily through parvocellular inputs, which mainly project to the ventral pathway, or through koniocellular inputs, which mainly project to the dorsal pathway. In the second and third experiments, shape sensitivity was observed, but in distinct spatio-temporal configurations from each other and from that elicited by grayscale inputs. Of particular interest, in the koniocellular condition, shape selectivity emerged earlier than in the parvocellular condition. These findings support the conclusion of distinct dorsal pathway computations of object shape, independent from the ventral pathway.

An evolving view in cognitive neuroscience is that the dorsal visual pathway not only plays a key role in visuomotor behavior but that it also contributes functionally to the recognition of objects. To characterize the nature of the object representations derived by the dorsal pathway, we assessed perceptual performance in the context of the continuous flash suppression paradigm, which suppresses object processing in the ventral pathway while sparing computation in the dorsal pathway. In a series of experiments, prime stimuli, which were rendered imperceptible by the continuous flash suppression, still contributed to perceptual decisions related to the subsequent perceptible target stimuli. However, the contribution of the prime to perception was contingent on the prime's structural coherence, in that a perceptual advantage was observed only for targets primed by objects with legitimate 3-D structure. Finally, we obtained additional evidence to demonstrate that the processing of the suppressed objects was contingent on the magnocellular, rather than the parvocellular, system, further linking the processing of the suppressed stimuli to the dorsal pathway. Together, these results provide novel evidence that the dorsal pathway does not only support visuomotor control but, rather, that it also derives the structural description of 3-D objects and contributes to shape perception.

Everyday objects are often composed of multiple parts, each with a unique surface texture. The neural substrates mediating the integration of surface features on different object parts are not fully understood, and potential contributions by both the ventral and dorsal visual pathways are possible. To explore these substrates, we collected fMRI data while human participants performed a difference detection task on two objects with textured parts. The objects could either differ in the assignment of the same texture to different object parts (“texture-location”) or the types of texture (“texture-type”). In the ventral stream, comparable BOLD activation levels were observed in response to texture-location and texture-type differences. In contrast, in a priori localized spatial processing regions of the dorsal stream, activation was greater for texture-location than texture-type differences, and the magnitude of the activation correlated with behavioral performance. We confirmed the reliance of surface texture to object part mapping on spatial processing mechanisms in subsequent psychophysical experiments, in which participants detected a difference in the spatial distance of an object relative to a reference line. In this task, distracter objects occasionally appeared, which differed in either texture-location or texture-type. Distracter texture-location differences slowed detection of spatial distance differences, but texture-type differences did not. More importantly, the distracter effects were only observed when texture-location differences were presented within whole shapes and not between separated shape parts at distinct spatial locations. We conclude that both the mapping of texture features to object parts and the representation of object spatial position are mediated by common neural substrates within the dorsal visual pathway.

It is commonly believed that, in right-handed individuals, words and faces are processed by distinct neural systems: one in the left hemisphere (LH) for words and the other in the right hemisphere (RH) for faces. Emerging evidence suggests, however, that hemispheric selectivity for words and for faces may not be independent of each other. One recent account suggests that words become lateralized to the LH to interact more effectively with language regions, and subsequently, as a result of competition with words for representational space, faces become lateralized to the RH. On this interactive account, left-handed individuals, who as a group show greater variability with respect to hemispheric language dominance, might be expected to show greater variability in their degree of RH lateralization of faces as well. The current study uses behavioral measures and ERPs to compare the hemispheric specialization for both words and faces in right- and left-handed adult individuals. Although both right- and left-handed groups demonstrated LH over RH superiority in discrimination accuracy for words, only the right-handed group demonstrated RH over LH advantage in discrimination accuracy for faces. Consistent with this, increased right-handedness was related to an increase in RH superiority for face processing, as measured by the strength of the N170 ERP component. Interestingly, the degree of RH behavioral superiority for face processing and the amplitude of the RH N170 for faces could be predicted by the magnitude of the N170 ERP response to words in the LH. These results are discussed in terms of a theoretical account in which the typical RH face lateralization fails to emerge in individuals with atypical language lateralization because of weakened competition from the LH representation of words.

Although object perception involves encoding a wide variety of object properties (e.g., size, color, viewpoint), some properties are irrelevant for identifying the object. The key to successful object recognition is having an internal representation of the object identity that is insensitive to these properties while accurately representing important diagnostic features. Behavioral evidence indicates that the formation of these kinds of invariant object representations takes many years to develop. However, little research has investigated the developmental emergence of invariant object representations in the ventral visual processing stream, particularly in the lateral occipital complex (LOC) that is implicated in object processing in adults. Here, we used an fMR adaptation paradigm to evaluate age-related changes in the neural representation of objects within LOC across variations in size and viewpoint from childhood through early adulthood. We found a dissociation between the neural encoding of object size and object viewpoint within LOC: by age of 5–10 years, area LOC demonstrates adaptation across changes in size, but not viewpoint, suggesting that LOC responses are invariant to size variations, but that adaptation across changes in view is observed in LOC much later in development. Furthermore, activation in LOC was correlated with behavioral indicators of view invariance across the entire sample, such that greater adaptation was correlated with better recognition of objects across changes in viewpoint. We did not observe similar developmental differences within early visual cortex. These results indicate that LOC acquires the capacity to compute invariance specific to different sources of information at different time points over the course of development.

The ability to recognize faces accurately and rapidly is an evolutionarily adaptive process. Most studies examining the neural correlates of face perception in adult humans have focused on a distributed cortical network of face-selective regions. There is, however, robust evidence from phylogenetic and ontogenetic studies that implicates subcortical structures, and recently, some investigations in adult humans indicate subcortical correlates of face perception as well. The questions addressed here are whether low-level subcortical mechanisms for face perception (in the absence of changes in expression) are conserved in human adults, and if so, what is the nature of these subcortical representations. In a series of four experiments, we presented pairs of images to the same or different eyes. Participants' performance demonstrated that subcortical mechanisms, indexed by monocular portions of the visual system, play a functional role in face perception. These mechanisms are sensitive to face-like configurations and afford a coarse representation of a face, comprised of primarily low spatial frequency information, which suffices for matching faces but not for more complex aspects of face perception such as sex differentiation. Importantly, these subcortical mechanisms are not implicated in the perception of other visual stimuli, such as cars or letter strings. These findings suggest a conservation of phylogenetically and ontogenetically lower-order systems in adult human face perception. The involvement of subcortical structures in face recognition provokes a reconsideration of current theories of face perception, which are reliant on cortical level processing, inasmuch as it bolsters the cross-species continuity of the biological system for face recognition.

Growing evidence suggests that the functional specialization of the two cortical visual pathways may not be as distinct as originally proposed. Here, we explore possible contributions of the dorsal “where/how” visual stream to shape perception and, conversely, contributions of the ventral “what” visual stream to location perception in human adults. Participants performed a shape detection task and a location detection task while undergoing fMRI. For shape detection, comparable BOLD activation in the ventral and dorsal visual streams was observed, and the magnitude of this activation was correlated with behavioral performance. For location detection, cortical activation was significantly stronger in the dorsal than ventral visual pathway and did not correlate with the behavioral outcome. This asymmetry in cortical profile across tasks is particularly noteworthy given that the visual input was identical and that the tasks were matched for difficulty in performance. We confirmed the asymmetry in a subsequent psychophysical experiment in which participants detected changes in either object location or shape, while ignoring the other, task-irrelevant dimension. Detection of a location change was slowed by an irrelevant shape change matched for difficulty, but the reverse did not hold. We conclude that both ventral and dorsal visual streams contribute to shape perception, but that location processing appears to be essentially a function of the dorsal visual pathway.

An age-related decline in face processing, even under conditions in which learning and memory are not implicated, has been well documented, but the mechanism underlying this perceptual alteration remains unknown. Here, we examine whether this behavioral change may be accounted for by a reduction in white matter connectivity with age. To this end, we acquired diffusion tensor imaging data from 28 individuals aged 18 to 86 years and quantified the number of fibers, voxels, and fractional anisotropy of the two major tracts that pass through the fusiform gyrus, the pre-eminent face processing region in the ventral temporal cortex. We also measured the ability of a subset of these individuals to make fine-grained discriminations between pairs of faces and between pairs of cars. There was a significant reduction in the structural integrity of the inferior fronto-occipital fasciculus (IFOF) in the right hemisphere as a function of age on all dependent measures and there were also some changes in the left hemisphere, albeit to a lesser extent. There was also a clear age-related decrement in accuracy of perceptual discrimination, especially for more challenging perceptual discriminations, and this held to a greater degree for faces than for cars. Of greatest relevance, there was a robust association between the reduction of IFOF integrity in the right hemisphere and the decline in face perception, suggesting that the alteration in structural connectivity between the right ventral temporal and frontal cortices may account for the age-related difficulties in face processing.

Specific regions of the human occipito-temporal cortex are consistently activated in functional imaging studies of face processing. To understand the contribution of these regions to face processing, we examined the pattern of fMRI activation in four congenital prosopagnosic (CP) individuals who are markedly impaired at face processing despite normal vision and intelligence, and with no evidence of brain damage. These individuals evinced a normal pattern of fMRI activation in the fusiform gyrus (FFA) and in other ventral occipito-temporal areas, in response to faces, buildings, and other objects, shown both as line drawings in detection and discrimination tasks and under more naturalistic testing conditions when no task was required. CP individuals also showed normal adaptation levels in a block-design adaptation experiment and, like control subjects, exhibited evidence of global face representation in the FFA. The absence of a BOLD-behavioral correlation (profound behavioral deficit, normal face-related activation in the ventral occipito-temporal cortex) challenges existing accounts of face representation, and suggests that activation in these cortical regions per se is not sufficient to ensure intact face processing.

We show that five individuals with congenital prosopagnosia (CP) are impaired at face recognition and discrimination and do not exhibit the normal superiority for upright over inverted faces despite intact visual acuity, low-level vision and intelligence, and in the absence of any obvious neural concomitant. Interestingly, the deficit is not limited to faces: The CP individuals were also impaired at discriminating common objects and novel objects although to a lesser extent than discriminating faces. The perceptual deficit may be attributable to a more fundamental visual processing disorder; the CP individuals exhibited difficulty in deriving global configurations from simple visual stimuli, even with extended exposure duration and considerable perceptual support in the image. Deriving a global configuration from local components is more critical for faces than for other objects, perhaps accounting for the exaggerated deficit in face processing. These findings elucidate the psychological mechanisms underlying CP and support the link between configural and face processing.

Agnosia, the impairment in object and face recognition despite intact vision and intelligence, is one of the most intriguing and debilitating neuropsychological deficits. The goal of this study was to determine whether S.M., an individual with longstanding visual agnosia and concomitant prosopagnosia, can be retrained to perform visual object recognition and, if so, what neural substrates mediate this reacquisition. Additionally, of interest is the extent to which training on one type of visual stimulus generalizes to other visual stimuli, as this informs our understanding of the organization of ventral visual cortex. Greebles were chosen as the stimuli for retraining given that, in neurologically normal individuals, these stimuli can engage the fusiform face area. Posttraining, S.M. showed significant improvement in recognizing Greebles, although he did not attain normal levels of performance. He was also able to recognize untrained Greebles and showed improvement in recognizing common objects. Surprisingly, his performance on face recognition, albeit poor initially, was even more impaired following training. A comparison of preand postintervention functional neuroimaging data mirrored the behavioral findings: Face-selective voxels in the fusiform gyrus prior to training were no longer so and were, in fact, more Greeble-selective. The findings indicate potential for experience-dependent dynamic reorganization in agnosia with the possibility that residual neural tissue, with limited capacity, will compete for representations.

Animal navigation studies have implicated structures in and around the hippocampal formation as crucial in performing path integration (a method of determining one's position by monitoring internally generated self-motion signals). Less is known about the role of these structures for human path integration. We tested path integration in patients who had undergone left or right medial temporal lobectomy as therapy for epilepsy. This procedure removed approximately 50% of the anterior portion of the hippocampus, as well as the amygdala and lateral temporal lobe. Participants attempted to walk without vision to a previously viewed target 2–6 m distant. Patients with right, but not left, hemisphere lesions exhibited both a decrease in the consistency of path integration and a systematic underregistration of linear displacement (and/or velocity) during walking. Moreover, the deficits were observable even when there were virtually no angular acceleration vestibular signals. The results suggest that structures in the medial temporal lobe participate in human path integration when individuals walk along linear paths and that this is so to a greater extent in right hemisphere structures than left. This information is relevant for future research investigating the neural substrates of navigation, not only in humans (e.g., functional neuroimaging and neuropsychological studies), but also in rodents and other animals.

The representations that mediate the coding of spatial position were examined by comparing the behavior of patients with left hemispatial neglect with that of nonneurological control subjects. To determine the spatial coordinate system(s) used to define “left” and “right,” eye movements were measured for targets that appeared at 58,108, and 158 to the relative left or right defined with respect to the midline of the eyes, head, or midsaggital plane of the trunk. In the baseline condition, in which the various egocentric midlines were all aligned with the environmental midline, patients were disproportionately slower at initiating saccades to left than right targets, relative to the controls. When either the trunk or the head was rotated and the midline aligned with the most peripheral position while the eyes remained aligned with the midline of the environment, the results did not differ from the baseline condition. However, when the eyes were rotated and the midline aligned with the peripheral position, saccadic reaction time (SRT) differed significantly from the baseline, especially when the eyes were rotated to the right. These findings suggest that target position is coded relative to the current position of gaze (oculocentrically) and that this eye-centered coding is modulated by orbital position (eye-in-head signal). The findings dovetail well with results from existing neurophysiological studies and shed further light on the spatial representations mediated by the human parietal cortex.

We argue that the current literature on prosopagnosia fails to demonstrate unequivocal evidence for a disproportionate impairment for faces as compared to nonface objects. Two prosopagnosic subjects were tested for the discrimination of objects from several categories (face as well as nonface) at different levels of categorization (basic, subordinate, and exemplar levels). Several dependent measures were obtained including accuracy, signal detection measures, and response times. The results from Experiments 1 to 4 demonstrate that, in simultaneous-matching tasks, response times may reveal impairments with nonface objects in subjects whose error rates only indicate a face deficit. The results from Experiments 5 and 6 show that, given limited stimulus presentation times for face and nonface objects, the same subjects may demonstrate a deªcit for both stimulus categories in sensitivity. In Experiments 7, 8 and 9, a match-to-sample task that places greater demands on memory led to comparable recognition sensitivity with both face and nonface objects. Regardless of object category, the prosopagnosic subjects were more affected by manipulations of the level of categorization than normal controls. This result raises questions regarding neuropsychological evidence for the modularity of face recognition, as well as its theoretical and methodological foundations.

In order to study face recognition in relative isolation from visual processes that may also contribute to object recognition and reading, we investigated CK, a man with normal face recognition but with object agnosia and dyslexia caused by a closed-head injury. We administered recognition tests of up right faces, of family resemblance, of age-transformed faces, of caricatures, of cartoons, of inverted faces, and of face features, of disguised faces, of perceptually degraded faces, of fractured faces, of faces parts, and of faces whose parts were made of objects. We compared CK's performance with that of at least 12 control participants. We found that CK performed as well as controls as long as the face was upright and retained the configurational integrity among the internal facial features, the eyes, nose, and mouth. This held regardless of whether the face was disguised or degraded and whether the face was represented as a photo, a caricature, a cartoon, or a face composed of objects. In the last case, CK perceived the face but, unlike controls, was rarely aware that it was composed of objects. When the face, or just the internal features, were inverted or when the configurational gestalt was broken by fracturing the face or misaligning the top and bottom halves, CK's performance suffered far more than that of controls. We conclude that face recognition normally depends on two systems: (1) a holistic, face-specific system that is dependent on orientationspecific coding of second-order relational features (internal), which is intact in CK and (2) a part-based object-recognition system, which is damaged in CK and which contributes to face recognition when the face stimulus does not satisfy the domain-specific conditions needed to activate the face system.

Unilateral parietal lobe damage, particularly in the right cerebral hemisphere, leads to neglect of stimuli on the contra lateral side. To determine the reference frame within which neglect operates in the somatosensory system, 11 patients with unilateral neglect were touched simultaneously on the left and right side of the wrist of one hand. The hand was tested in both the palm up and the palm down position. Patients neglected the stimuli on the side of space contra lateral to the lesion regardless of hand position. These results indicate that point-localization in the somatosensory system is accomplished with respect to a spatially defined frame-of-reference and not strictly with respect to somatotopically defined coordinates.