We proposed a theory of consciousness in which the machinery for social perception constructs awareness, and awareness is a perceptual model of the process of attention. One can attribute awareness to others or to oneself. Awareness of X is the brain's perceptual metaphor for the deep attentive processing of X. A set of ten comments on our hypothesis are included in this issue. Each comment raises specific points some of which directly challenge the hypothesis. Here we respond to these specific points and challenges.

Macaque anatomy and physiology studies have revealed multiple visual areas in posterior parietal cortex (PPC). While many response properties of PPC neurons have been probed, little is known about PPC's large-scale functional topography-specifically related to visuotopic organization. Using high-resolution functional magnetic resonance imaging at 3 T with a phase-encoded retinotopic mapping paradigm in the awake macaque, a large-scale visuotopic organization along lateral portions of PPC anterior to area V3a and extending into the lateral intraparietal sulcus (LIP) was found. We identify two new visual field maps anterior to V3a within caudal PPC, referred to as caudal intraparietal-1 (CIP-1) and CIP-2. The polar angle representation in CIP-1 extends from regions near the upper vertical meridian (that is the shared border with V3a and dorsal prelunate) to those within the lower visual field (that is the shared border with CIP-2). The polar angle representation in CIP-2 is a mirror reversal of the CIP-1 representation. CIP-1 and CIP-2 share a representation of central space on the lateral border. Anterior to CIP-2, a third polar angle representation was found within LIP, referred to as visuotopic LIP. The polar angle representation in LIP extends from regions near the upper vertical meridian (that is the shared border with CIP-2) to those near the lower vertical meridian. Representations of central visual space were identified within dorsal portions of LIP with peripheral representations in ventral portions. We also consider the topographic large-scale organization found within macaque PPC relative to that observed in human PPC.

Multiple stimuli present in the visual field at the same time compete for neural representation by mutually suppressing their evoked activity throughout visual cortex, providing a neural correlate for the limited processing capacity of the visual system. Competitive interactions among stimuli can be counteracted by top-down, goal-directed mechanisms such as attention, and by bottom-up, stimulus-driven mechanisms. Because these two processes cooperate in everyday life to bias processing toward behaviorally relevant or particularly salient stimuli, it has proven difficult to study interactions between top-down and bottom-up mechanisms. Here, we used an experimental paradigm in which we first isolated the effects of a bottom-up influence on neural competition by parametrically varying the degree of perceptual grouping in displays that were not attended. Second, we probed the effects of directed attention on the competitive interactions induced with the parametric design. We found that the amount of attentional modulation varied linearly with the degree of competition left unresolved by bottom-up processes, such that attentional modulation was greatest when neural competition was little influenced by bottom-up mechanisms and smallest when competition was strongly influenced by bottom-up mechanisms. These findings suggest that the strength of attentional modulation in the visual system is constrained by the degree to which competitive interactions have been resolved by bottom-up processes related to the segmentation of scenes into candidate objects.

A common modern view of consciousness is that it is an emergent property of the brain, perhaps caused by neuronal complexity, and perhaps with no adaptive value. Exactly what emerges, how it emerges, and from what specific neuronal process, is in debate. One possible explanation of consciousness, proposed here, is that it is a construct of the social perceptual machinery. Humans have specialized neuronal machinery that allows us to be socially intelligent. The primary role for this machinery is to construct models of other people's minds thereby gaining some ability to predict the behavior of other individuals. In the present hypothesis, awareness is a perceptual reconstruction of attentional state; and the machinery that computes information about other people's awareness is the same machinery that computes information about our own awareness. The present article brings together a variety of lines of evidence including experiments on the neural basis of social perception, on hemispatial neglect, on the out-of-body experience, on mirror neurons, and on the mechanisms of decision-making, to explore the possibility that awareness is a construct of the social machinery in the brain.

Theories of spatial attentional control have been largely based upon studies of patients suffering from visuospatial neglect, resulting from circumscribed lesions of frontal and posterior parietal cortex. In the intact brain, the control of spatial attention has been related to a distributed frontoparietal attention network. Little is known about the nature of the control mechanisms exerted by this network. Here, we used a novel region-of-interest approach to relate activations of the attention network to recently described topographic areas in frontal cortex [frontal eye field (FEF), PreCC/IFS (precentral cortex/inferior frontal sulcus)] and parietal cortex [intraparietal sulcus areas (IPS1-IPS5) and an area in the superior parietal lobule (SPL1)] to examine their spatial attention signals. We found that attention signals in most topographic areas were spatially specific, with stronger responses when attention was directed to the contralateral than to the ipsilateral visual field. Importantly, two hemispheric asymmetries were found. First, a region in only right, but not left SPL1 carried spatial attention signals. Second, left FEF and left posterior parietal cortex (IPS1/2) generated stronger contralateral biasing signals than their counterparts in the right hemisphere. These findings are the first to characterize spatial attention signals in topographic frontal and parietal cortex and provide a neural basis in support of an interhemispheric competition account of spatial attentional control.

Multiple stimuli that are present simultaneously in the visual field compete for neural representation. At the same time, however, multiple stimuli in cluttered scenes also undergo perceptual organization according to certain rules originally defined by the Gestalt psychologists such as similarity or proximity, thereby segmenting scenes into candidate objects. How can these two seemingly orthogonal neural processes that occur early in the visual processing stream be reconciled? One possibility is that competition occurs among perceptual groups rather than at the level of elements within a group. We probed this idea using fMRI by assessing competitive interactions across visual cortex in displays containing varying degrees of perceptual organization or perceptual grouping (Grp). In strong Grp displays, elements were arranged such that either an illusory figure or a group of collinear elements were present, whereas in weak Grp displays the same elements were arranged randomly. Competitive interactions among stimuli were overcome throughout early visual cortex and V4, when elements were grouped regardless of Grp type. Our findings suggest that context-dependent grouping mechanisms and competitive interactions are linked to provide a bottom-up bias toward candidate objects in cluttered scenes.

Abstract In his article, Lamme provides a neurotheoretical argument that recurrent processing (RP) produces the phenomenological sensations that form the contents of our conscious experiences. Importantly, he argues that this processing includes local intra-areal (i.e., horizontal connections) as well as local inter-areal feedback (i.e., from higher level sensory areas to lower level ones) interactions that occur within the sensory cortices. This has direct implications for what the contents of these experiences may be and the role that neuroscience can play in identifying them.

In order to investigate the search performance and strategies of nonhuman primates, two macaque monkeys were trained to search for a target template among differently oriented distractors in both free-gaze and fixed-gaze viewing conditions (overt and covert search). In free-gaze search, reaction times (RT) and eye movements revealed the theoretically predicted characteristics of exhaustive and self-terminating serial search, with certain exceptions that are also observed in humans. RT was linearly related to the number of fixations but not necessarily to the number of items on display. Animals scanned the scenes in a nonrandom manner spending notably more time on targets and items inspected last (just before reaction). The characteristics of free-gaze search were then compared with search performance under fixed gaze (covert search) and with the performance of four human subjects tested in similar experiments. By and large the performance characteristics of both groups were similar; monkeys were slightly faster, and humans more accurate. Both species produced shorter RT in fixed-gaze than in free-gaze search. But while RT slopes of the human subjects still showed the theoretically predicted difference between hits and rejections, slopes of the two monkeys appeared to collapse. Despite considerable priming and short-term learning when similar tests were continuously repeated, no substantial long-term training effects were seen when test conditions and set sizes were frequently varied. Altogether, the data reveal many similarities between human and monkey search behavior but indicate that search is not necessarily restricted to exclusively serial processes.

Functional magnetic resonance imaging studies have shown that human ventral visual cortex anterior to human visual area V4 contains two visual field maps, VO-1 and VO-2, that together form the ventral occipital (VO) cluster (Brewer et al., 2005). This cluster is characterized by common functional response properties and responds preferentially to color and object stimuli. Here, we confirm the topographic and functional characteristics of the VO cluster and describe two new visual field maps that are located anterior to VO-2 extending across the collateral sulcus into the posterior parahippocampal cortex (PHC). We refer to these visual field maps as parahippocampal areas PHC-1 and PHC-2. Each PHC map contains a topographic representation of contralateral visual space. The polar angle representation in PHC-1 extends from regions near the lower vertical meridian (that is the shared border with VO-2) to those close to the upper vertical meridian (that is the shared border with PHC-2). The polar angle representation in PHC-2 is a mirror reversal of the PHC-1 representation. PHC-1 and PHC-2 share a foveal representation and show a strong bias toward representations of peripheral eccentricities. Both the foveal and peripheral representations of PHC-1 and PHC-2 respond more strongly to scenes than to objects or faces, with greater scene preference in PHC-2 than PHC-1. Importantly, both areas heavily overlap with the functionally defined parahippocampal place area. Our results suggest that ventral visual cortex can be subdivided on the basis of topographic criteria into a greater number of discrete maps than previously thought.

In this issue of Neuron, Mahon et al. show that the ventral visual cortex of congenitally blind individuals, who have never experienced the visual world, has an object-category organization similar to that found in sighted individuals. Here, we discuss the implications of this finding for our understanding of the "visual" cortex.

The thalamus has traditionally been thought to passively relay sensory information to the cortex. By showing that responses in visual thalamus are modulated by perceptual and cognitive tasks, recent fMRI and physiology studies have helped revise this view. The modulatory input to the visual thalamus derives from functionally distinct cortical and subcortical feedback pathways. These pathways enable the lateral geniculate nucleus and pulvinar to regulate the information transmitted to cortical areas according to cognitive requirements. Emerging evidence suggests that such regulation involves changing the degree of synchrony between neurons as well as changing the magnitude of thalamic activity. These findings support a role for the thalamus that extends as far as contributing to the control of visual attention and awareness.

The visual system has an extraordinary capability to extract categorical information from complex natural scenes. For example, subjects are able to rapidly detect the presence of object categories such as animals or vehicles in new scenes that are presented very briefly. This is even true when subjects do not pay attention to the scenes and simultaneously perform an unrelated attentionally demanding task, a stark contrast to the capacity limitations predicted by most theories of visual attention. Here we show a neural basis for rapid natural scene categorization in the visual cortex, using functional magnetic resonance imaging and an object categorization task in which subjects detected the presence of people or cars in briefly presented natural scenes. The multi-voxel pattern of neural activity in the object-selective cortex evoked by the natural scenes contained information about the presence of the target category, even when the scenes were task-irrelevant and presented outside the focus of spatial attention. These findings indicate that the rapid detection of categorical information in natural scenes is mediated by a category-specific biasing mechanism in object-selective cortex that operates in parallel across the visual field, and biases information processing in favour of objects belonging to the target object category.

Limits to the capacity of visual short-term memory (VSTM) indicate a maximum storage of only 3 or 4 items. Recently, it has been suggested that activity in a specific part of the brain, the posterior parietal cortex (PPC), is correlated with behavioral estimates of VSTM capacity and might reflect a capacity-limited store. In three experiments that varied the delay period and the stimuli to be stored, we found dissociations between functional magnetic resonance imaging (fMRI) activity in PPC and behavioral measures of capacity. When the delay length increased, fMRI activity in this area increased with memory load beyond the behaviorally determined limits of capacity. The results suggest that activity in PPC may reflect the attentional demands of short-term memory rehearsal processes rather than capacity limitations, and imply that a larger number of items than that determined by behavioral measures of capacity may be rehearsed during STM tasks. This account is consistent with the role of PPC in attentional processes and with the close correlation between brain areas that are involved in attention and those that mediate STM.

Single-cell studies in the macaque have reported selective neural responses evoked by visual presentations of faces and bodies. Consistent with these findings, functional magnetic resonance imaging studies in humans and monkeys indicate that regions in temporal cortex respond preferentially to faces and bodies. However, it is not clear how these areas correspond across the two species. Here, we directly compared category-selective areas in macaques and humans using virtually identical techniques. In the macaque, several face- and body part-selective areas were found located along the superior temporal sulcus (STS) and middle temporal gyrus (MTG). In the human, similar to previous studies, face-selective areas were found in ventral occipital and temporal cortex and an additional face-selective area was found in the anterior temporal cortex. Face-selective areas were also found in lateral temporal cortex, including the previously reported posterior STS area. Body part-selective areas were identified in the human fusiform gyrus and lateral occipitotemporal cortex. In a first experiment, both monkey and human subjects were presented with pictures of faces, body parts, foods, scenes, and man-made objects, to examine the response profiles of each category-selective area to the five stimulus types. In a second experiment, face processing was examined by presenting upright and inverted faces. By comparing the responses and spatial relationships of the areas, we propose potential correspondences across species. Adjacent and overlapping areas in the macaque anterior STS/MTG responded strongly to both faces and body parts, similar to areas in the human fusiform gyrus and posterior STS. Furthermore, face-selective areas on the ventral bank of the STS/MTG discriminated both upright and inverted faces from objects, similar to areas in the human ventral temporal cortex. Overall, our findings demonstrate commonalities and differences in the wide-scale brain organization between the two species and provide an initial step toward establishing functionally homologous category-selective areas.

The role of subcortical visual structures such as the lateral geniculate nucleus (LGN) and the superior colliculus (SC) in the control of visual spatial attention remains poorly understood. Here, we used high-resolution functional magnetic resonance imaging to measure responses in the human LGN and SC during sustained spatial attention. Subjects covertly and continuously tracked one of two segments that rotated through the visual field, composed of either moving dots or transient colored shapes. Activity in both nuclei was generally enhanced by attention, independent of the stimulus type, with the voxels responding more sensitively to stimulus contrast (those dominated by magnocellular input) exhibiting greater attentional enhancement. The LGN contained clusters of voxels exhibiting attentional enhancement or weak suppression, whereas the SC exhibited predominantly attentional enhancement, which was significantly stronger than in the LGN. The spatial distribution of the attentional effects was unrelated to the retinotopic organization in either structure. The results demonstrate that each of the major subcortical visual pathways participates in attentional selection, and their differential magnitudes of modulation suggest distinct roles.

Transcranial magnetic stimulation (TMS) is an established technique in cognitive neuroscience which is used to interrupt processing in the brain, creating a brief 'virtual lesion'. Here, we review recent studies that have employed TMS to gain insight into the roles of frontal and parietal cortex in visuospatial attention control.

A traditional view of the human motor cortex is that it contains an overlapping sequence of body part representations from the tongue in a ventral location to the foot in a dorsal location. In this study, high-resolution functional MRI (1.5x1.5x2 mm) was used to examine the somatotopic map in the lateral motor cortex of humans, to determine whether it followed the traditional somatotopic order or whether it contained any violations of that somatotopic order. The arm and hand representation had a complex organization in which the arm was relatively emphasized in two areas: one dorsal and the other ventral to a region that emphasized the fingers. This violation of a traditional somatotopic order suggests that the motor cortex is not merely a map of the body but is topographically shaped by other influences, perhaps including correlations in the use of body parts in the motor repertoire.

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.

Recent imaging studies have shown that the human posterior parietal cortex (PPC) contains four topographically organized areas along the intraparietal sulcus (IPS1-IPS4). Using a memory-guided saccade paradigm, we confirmed the locations and retinotopic organization of IPS1-IPS4 and identified two additional areas, IPS5 and superior parietal lobule 1 (SPL1). IPS5 is located at the intersection of the intraparietal and postcentral sulcus; SPL1 branches off the IPS and extends into the superior parietal lobule. Both areas, as well as IPS1-IPS4, each contain a representation of the contralateral visual hemifield. We then probed core functions of the dorsal pathway in these areas, that is, the representation of eye movements and visual motion, to compare the functional characteristics of human PPC to physiologically and anatomically defined areas in monkey PPC. First, as in monkey PPC, a gradient representation of eye movements was found along the IPS with decreasing responses for saccades and increasing responses for smooth pursuit eye movements from posterior/medial to anterior/lateral. The greatest preference for saccades was found in SPL1 and for smooth pursuit in IPS5. Second, and again similar to monkey PPC, all topographically organized PPC areas responded to different types of motion including planar, circular, and radial optic flow, as assessed using adaptation paradigms. Areas in posterior IPS preferred radial optic flow over planar motion, whereas areas in anterior PPC did not show preference for a particular motion type. Together, our results indicate strikingly similar characteristics in the general functional organization of human and monkey PPC, but also reveal some notable differences.

Selective attention modulates neural activity in the visual system both in the presence and in the absence of visual stimuli. When subjects direct attention to a particular location in a visual scene in anticipation of the stimulus onset, there is an increase in baseline activity. How do such baseline increases relate to the attentional modulation of stimulus-driven activity? Using functional magnetic resonance imaging, we demonstrate that baseline increases related to the expectation of motion or color stimuli at a peripheral target location do not predict the modulation of neural responses evoked by these stimuli when attended. In areas such as MT and TEO that were more effectively activated by one stimulus type than the other, attentional modulation of visually evoked activity depended on the stimulus preference of a visual area and was stronger for the effective than for the noneffective stimulus. In contrast, baseline increases did not reflect the stimulus preference of a visual area. Rather, these signals were shown to be spatially specific and appeared to be dominated by the location information and not by the feature information of the cue with the experimental paradigms under study. These findings provide evidence that baseline increases in visual cortex during cue periods do not reflect the activation of a memory template that includes particular stimulus properties of the expected target, but rather carry information about the location of an expected target stimulus. In addition, when the stimulus contained both color and motion, an object-based attention effect was observed, with significant attentional modulation in the area that responded preferentially to the unattended feature.

We used fMRI at 3 Tesla and improved spatial resolution (2 x 2 x 2 mm(3)) to investigate topographic organization in human frontal cortex using memory-guided response tasks performed at 8 or 12 peripheral locations arranged clockwise around a central fixation point. The tasks required the location of a peripheral target to be remembered for several seconds after which the subjects either made a saccade to the remembered location (memory-guided saccade task) or judged whether a test stimulus appeared in the same or a slightly different location by button press (spatial working-memory task). With these tasks, we found two topographic maps in each hemisphere, one in the superior branch of precentral cortex and caudalmost part of the superior frontal sulcus, in the region of the human frontal eye field, and a second in the inferior branch of precentral cortex and caudalmost part of the inferior frontal sulcus, both of which greatly overlapped with activations evoked by visually guided saccades. In each map, activated voxels coded for saccade directions and memorized locations predominantly in the contralateral hemifield with neighboring saccade directions and memorized locations represented in adjacent locations of the map. Particular saccade directions or memorized locations were often represented in multiple locations of the map. The topographic activation patterns showed individual variability from subject to subject but were reproducible within subjects. Notably, only saccade-related activation, but no topographic organization, was found in the region of the human supplementary eye field in dorsomedial prefrontal cortex. Together these results show that topographic organization can be revealed outside sensory cortical areas using more complex behavioral tasks.

The lateral geniculate nucleus (LGN) is the thalamic station in the retinocortical projection and has traditionally been viewed as the gateway for sensory information to enter the cortex. Here, we review recent studies of the human LGN that have investigated the retinotopic organization, physiologic response properties, and modulation of neural activity by selective attention and by visual awareness in a binocular rivalry paradigm. In the retinotopy studies, we found that the contralateral visual field was represented with the lower field in the medial-superior portion and the upper field in the lateral-inferior portion of each LGN. The fovea was represented in posterior and superior portions, with increasing eccentricities represented more anteriorly. Functional MRI responses increased monotonically with stimulus contrast in the LGN and in visual cortical areas. In the LGN, the dynamic response range of the contrast function was larger and contrast gain was lower than in the cortex. In our attention studies, we found that directed attention to a spatial location modulated neural activity in the LGN in several ways: it enhanced neural responses to attended stimuli, attenuated responses to ignored stimuli, and increased baseline activity in the absence of visual stimulation. Furthermore, we showed in a binocular rivalry paradigm that neural activity in the LGN correlated strongly with the subjects' reported percepts. The overall view that emerges from these studies is that the human LGN plays a role in perception and cognition far beyond that of a relay nucleus and, rather, needs to be considered as an early gatekeeper in the control of visual attention and awareness.

Methods for performing functional magnetic resonance imaging (fMRI) studies in behaving and lesioned monkeys using a human MR scanner are reported. Materials for head implant surgery were selected based on tests for magnetic susceptibility. A primate chair with a rigid head fixation system and a mock scanner environment for training were developed. To perform controlled visual studies, monkeys were trained to maintain fixation for several minutes using a novel training technique that utilized continuous juice rewards. A surface coil was used to acquire anatomical and functional images in four monkeys, one with a partial lesion of striate cortex. High-resolution anatomical images were used after non-uniform intensity correction to create cortical surface reconstructions of both lesioned and normal hemispheres. Our methods were confirmed in two visual experiments, in which functional activations were obtained during both free viewing and fixation conditions. In one experiment, face-selective activity was found in the fundus and banks of the superior temporal sulcus and the middle temporal gyrus in monkeys viewing pictures of faces and objects while maintaining fixation. In a second experiment, regions in occipital, parietal, and frontal cortex were activated in lesioned and normal animals viewing a cartoon movie. Importantly, in the animal with the striate lesion, fMRI signals were obtained in the immediate vicinity of the lesion. Our results extend those previously reported by providing a detailed account of the technique and by demonstrating the feasibility of fMRI in monkeys with lesions.

When dissimilar images are presented to the two eyes, they compete for perceptual dominance so that only one image is visible at a time while the other one is suppressed. Neural correlates of such binocular rivalry have been found at multiple stages of visual processing, including striate and extrastriate visual cortex. However, little is known about the role of subcortical processing during binocular rivalry. Here we used fMRI to measure neural activity in the human LGN while subjects viewed contrast-modulated gratings presented dichoptically. Neural activity in the LGN correlated strongly with the subjects' reported percepts, such that activity increased when a high-contrast grating was perceived and decreased when a low-contrast grating was perceived. Our results provide evidence for a functional role of the LGN in binocular rivalry and suggest that the LGN, traditionally viewed as the gateway to the visual cortex, may be an early gatekeeper of visual awareness.

The human ability to detect symmetry has been a topic of interest to psychologists and philosophers since the 19th century, yet surprisingly little is known about the neural basis of symmetry perception. In a recent fMRI study, Sasaki and colleagues begin to remedy this situation. By identifying the neural structures that respond to symmetry in both humans and macaques, the authors lay the groundwork for understanding the neural mechanisms underlying symmetry perception.

When multiple stimuli appear simultaneously in the visual field, they are not processed independently, but rather interact in a mutually suppressive way, suggesting that they compete for neural representation in visual cortex. The biased competition model of selective attention predicts that the competition can be influenced by both top-down and bottom-up mechanisms. Directed attention has been shown to bias competition in favor of the attended stimulus in extrastriate cortex. Here, we show that suppressive interactions among multiple stimuli are eliminated in extrastriate cortex when they are presented in the context of pop-out displays, in which a single item differs from the others, but not in heterogeneous displays, in which all items differ from each other. The pop-out effects seemed to originate in early visual cortex and were independent of attentional top-down control, suggesting that stimulus context may provide a powerful influence on neural competition in human visual cortex.

The superior colliculus (SC) is a multimodal laminar structure located on the roof of the brain stem. The SC is a key structure in a distributed network of areas that mediate saccadic eye movements and shifts of attention across the visual field and has been extensively studied in nonhuman primates. In humans, it has proven difficult to study the SC with functional MRI (fMRI) because of its small size, deep location, and proximity to pulsating vascular structures. Here, we performed a series of high-resolution fMRI studies at 3 T to investigate basic visual response properties of the SC. The retinotopic organization of the SC was determined using the traveling wave method with flickering checkerboard stimuli presented at different polar angles and eccentricities. SC activations were confined to stimulation of the contralateral hemifield. Although a detailed retinotopic map was not observed, across subjects, the upper and lower visual fields were represented medially and laterally, respectively. Responses were dominantly evoked by stimuli presented along the horizontal meridian of the visual field. We also measured the sensitivity of the SC to luminance contrast, which has not been previously reported in primates. SC responses were nearly saturated by low contrast stimuli and showed only small response modulation with higher contrast stimuli, indicating high sensitivity to stimulus contrast. Responsiveness to stimulus motion in the SC was shown by robust activations evoked by moving versus static dot stimuli that could not be attributed to eye movements. The responses to contrast and motion stimuli were compared with those in the human lateral geniculate nucleus. Our results provide first insights into basic visual responses of the human SC and show the feasibility of studying subcortical structures using high-resolution fMRI.

Human neuroimaging studies suggest that areas in temporal cortex respond preferentially to certain biologically relevant stimulus categories such as faces and bodies. Single-cell studies in monkeys have reported cells in inferior temporal cortex that respond selectively to faces, hands, and bodies but provide little evidence of large clusters of category-specific cells that would form "areas." We probed the category selectivity of macaque temporal cortex for representations of monkey faces and monkey body parts relative to man-made objects using functional MRI in animals trained to fixate. Two face-selective areas were activated bilaterally in the posterior and anterior superior temporal sulcus exhibiting different degrees of category selectivity. The posterior face area was more extensively activated in the right hemisphere than in the left hemisphere. Immediately adjacent to the face areas, regions were activated bilaterally responding preferentially to body parts. Our findings suggest a category-selective organization for faces and body parts in macaque temporal cortex.

Natural visual scenes are cluttered and contain many different objects that cannot all be processed simultaneously. Therefore, attentional mechanisms are needed to select relevant and to filter out irrelevant information. Evidence from functional brain imaging reveals that attention operates at various processing levels within the visual system and beyond. First, the lateral geniculate nucleus appears to be the first stage in the processing of visual information that is modulated by attention, consistent with the idea that it may play an important role as an early gatekeeper in controlling neural gain. Second, areas at intermediate cortical-processing levels, such as V4 and TEO, appear to be important sites at which attention filters out unwanted information by means of receptive field mechanisms. Third, the attention mechanisms that operate in the visual system appear to be controlled by a distributed network of higher order areas in the frontal and parietal cortex, which generate top-down signals that are transmitted via feedback connections to the visual system. And fourth, the pulvinar of the thalamus may operate by integrating and coordinating attentional functions in concert with the fronto-parietal network, although much needs to be learned about its functional properties. The overall view that emerges from the studies reviewed in this article is that neural mechanisms of selective attention operate at multiple stages in the visual system and beyond and are determined by the visual processing capabilities of each stage. In this respect, attention can be considered in terms of a multilevel selection process.

Functional magnetic resonance imaging (fMRI) has provided intriguing insights into the topography and functional organization of visual cortical areas in the human brain. However, little is known about the functional anatomy of subcortical nuclei. Here, we used high-resolution fMRI (1.5 x 1.5 x 2 mm3) at 3 tesla to investigate the retinotopic organization of the human lateral geniculate nucleus (LGN). The central 15 degrees of the visual field were mapped using periodic flickering checkerboard stimuli that evoked a traveling wave of activity. The contralateral visual hemifield was represented with the lower field in the medial-superior portion and the upper field in the lateral-inferior portion of each LGN. The horizontal meridian was significantly overrepresented relative to the vertical meridian. The fovea was represented in posterior and superior portions, with increasing eccentricities represented more anteriorly. The magnification of the fovea relative to the periphery was similar to that described for human primary visual cortex. The magnocellular regions of the LGN were distinguished based on their sensitivity to low stimulus contrast and tended to be located in its inferior and medial portions. Our results demonstrate striking similarities in the topographic organization of the macaque and human LGN and support accounts of a constant magnification from the retina through the cortex in both species.

Selective attention operates in visual cortex by facilitating processing of selected stimuli and by filtering out unwanted information from nearby distracters over circumscribed regions of visual space. The neural representation of unattended stimuli outside this focus of attention is less well understood. We studied the neural fate of unattended stimuli using functional magnetic resonance imaging by dissociating the activity evoked by attended (target) stimuli presented to the periphery of a visual hemifield and unattended (distracter) stimuli presented simultaneously to a corresponding location of the contralateral hemifield. Subjects covertly directed attention to a series of target stimuli and performed either a low or a high attentional-load search task on a stream of otherwise identical stimuli. With this task, target-search-related activity increased with increasing attentional load, whereas distracter-related activity decreased with increasing load in areas V4 and TEO but not in early areas V1 and V2. This finding presents evidence for a load-dependent push-pull mechanism of selective attention that operates over large portions of the visual field at intermediate processing stages. This mechanism appeared to be controlled by a distributed frontoparietal network of brain areas that reflected processes related to target selection during spatially directed attention.

In the human brain, little is known about the functional anatomy and response properties of subcortical nuclei containing visual maps such as the lateral geniculate nucleus (LGN) and the pulvinar. Using functional magnetic resonance imaging (fMRI) at 3 tesla (T), collective responses of neural populations in the LGN were measured as a function of stimulus contrast and flicker reversal rate and compared with those obtained in visual cortex. Flickering checkerboard stimuli presented in alternation to the right and left hemifields reliably activated the LGN. The peak of the LGN activation was found to be on average within +/-2 mm of the anatomical location of the LGN, as identified on high-resolution structural images. In all visual areas except the middle temporal (MT), fMRI responses increased monotonically with stimulus contrast. In the LGN, the dynamic response range of the contrast function was larger and contrast gain was lower than in the cortex. Contrast sensitivity was lowest in the LGN and V1 and increased gradually in extrastriate cortex. In area MT, responses were saturated at 4% contrast. Response modulation by changes in flicker rate was similar in the LGN and V1 and occurred mainly in the frequency range between 0.5 and 7.5 Hz; in contrast, in extrastriate areas V4, V3A, and MT, responses were modulated mainly in the frequency range between 7.5 and 20 Hz. In the human pulvinar, no activations were obtained with the experimental designs used to probe response properties of the LGN. However, regions in the mediodorsal right and left pulvinar were found to be consistently activated by bilaterally presented flickering checkerboard stimuli, when subjects attended to the stimuli. Taken together, our results demonstrate that fMRI at 3 T can be used effectively to study thalamocortical circuits in the human brain.

In recordings from two awake, behaving macaque monkeys we found that neurons in the crown of the prelunate gyrus differed in their responsiveness to simple visual stimuli. Neurons in the posterior part of the gyrus (area V4) responded strongly to stationary or moving bars, while neurons in the anterior part (area V4A) responded only weakly to such stimuli. Most receptive fields in area V4A were elongated with long axes oriented radially towards the fovea. These neurons were sensitive to radial movements, especially to sudden shifts of real 3D objects. The border between areas V4 and V4A coincided with the representation of the horizontal meridian. Area V4A extended into the posterior bank of the superior temporal sulcus, where its border corresponded to the representation of the vertical meridian. The sequence of the representations of the horizontal and vertical meridians over the prelunate gyrus suggests the existence of another area between V4A and V4t.

A typical scene contains many different objects that compete for neural representation due to the limited processing capacity of the visual system. At the neural level, competition among multiple stimuli is evidenced by the mutual suppression of their visually evoked responses and occurs most strongly at the level of the receptive field. The competition among multiple objects can be biased by both bottom-up sensory-driven mechanisms and top-down influences, such as selective attention. Functional brain imaging studies reveal that biasing signals due to selective attention can modulate neural activity in visual cortex not only in the presence but also in the absence of visual stimulation. Although the competition among stimuli for representation is ultimately resolved within visual cortex, the source of top-down biasing signals likely derives from a distributed network of areas in frontal and parietal cortex. Competition suggests that once attentional resources are depleted, no further processing is possible. Yet, existing data suggest that emotional stimuli activate brain regions "automatically," largely immune from attentional control. We tested the alternative possibility, namely, that the neural processing of stimuli with emotional content is not automatic and instead requires some degree of attention. Our results revealed that, contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, similar to the processing of other stimulus categories, the processing of facial expression is under top-down control.

Attentional mechanisms are important for selecting relevant information and filtering out irrelevant information from cluttered visual scenes. Selective attention has previously been shown to affect neural activity in both extrastriate and striate visual cortex. Here, evidence from functional brain imaging shows that attentional response modulation is not confined to cortical processing, but can occur as early as the thalamic level. We found that attention modulated neural activity in the human lateral geniculate nucleus (LGN) in several ways: it enhanced neural responses to attended stimuli, attenuated responses to ignored stimuli and increased baseline activity in the absence of visual stimulation. The LGN, traditionally viewed as the gateway to visual cortex, may also serve as a 'gatekeeper' in controlling attentional response gain.

In single-cell recordings from the dorsocaudal part of the prelunate gyrus of an alert monkey (Macaca fascicularis) we found neurons with unexpectedly large receptive fields (RFs) that spread bilaterally into the contra- and ipsilateral visual fields. These neurons (n=82) appeared to be clustered in the periphery of V4. They were surrounded by neurons with relatively small (3-10 degrees) and unilateral RFs in the contralateral field with properties similar to those previously described for neurons in area V4. Bilateral RFs extended over large parts of the lower visual field but always spared the fovea. Receptive fields typically revealed two foci of maximal responsiveness that were arranged symmetrically in the ipsi- and contralateral fields. Twenty-six cells did not respond to stimuli along the vertical meridian; these neurons had two distinct RFs. The preference for stimulus orientation, color, or motion was similar in all parts of these large RFs.

A typical scene contains many different objects that compete for neural representation due to the limited processing capacity of the visual system. At the neural level, competition among multiple stimuli is evidenced by the mutual suppression of their visually evoked responses and occurs most strongly at the level of the receptive field. The competition among multiple objects can be biased by both bottom-up sensory-driven mechanisms and top-down influences, such as selective attention. Functional brain imaging studies reveal that biasing signals due to selective attention can modulate neural activity in visual cortex not only in the presence, but also in the absence of visual stimulation. Although the competition among stimuli for representation is ultimately resolved within visual cortex, the source of top-down biasing signals likely derives from a distributed network of areas in frontal and parietal cortex. Attention-related activity in frontal and parietal areas does not reflect attentional modulation of visually evoked responses, but rather the attentional operations themselves.

Neurophysiological studies in monkeys show that when multiple visual stimuli appear simultaneously in the visual field, they are not processed independently, but rather interact in a mutually suppressive way. This suggests that multiple stimuli compete for neural representation. Consistent with this notion, we have previously found in humans that functional magnetic resonance imaging (fMRI) signals in V1 and ventral extrastriate areas V2, V4, and TEO are smaller for simultaneously presented (i.e., competing) stimuli than for the same stimuli presented sequentially (i.e., not competing). Here we report that suppressive interactions between stimuli are also present in dorsal extrastriate areas V3A and MT, and we compare these interactions to those in areas V1 through TEO. To exclude the possibility that the differences in responses to simultaneously and sequentially presented stimuli were due to differences in the number of transient onsets, we tested for suppressive interactions in area V4, in an experiment that held constant the number of transient onsets. We found that the fMRI response to a stimulus in the upper visual field was suppressed by the presence of nearby stimuli in the lower visual field. Further, we excluded the possibility that the greater fMRI responses to sequential compared with simultaneous presentations were due to exogeneous attentional cueing by having our subjects count T's or L's at fixation, an attentionally demanding task. Behavioral testing demonstrated that neither condition interfered with performance of the T/L task. Our previous findings suggested that suppressive interactions among nearby stimuli in areas V1 through TEO were scaled to the receptive field (RF) sizes of neurons in those areas. Here we tested this idea by parametrically varying the spatial separation among stimuli in the display. Display sizes ranged from 2 x 2 degrees to 7 x 7 degrees and were centered at 5.5 degrees eccentricity. Based on the effects of display size on the magnitude of suppressive interactions, we estimated that RF sizes at an eccentricity of 5.5 degrees were <2 degrees in V1, 2-4 degrees in V2, 4-6 degrees in V4, larger than 7 degrees (but still confined to a quadrant) in TEO, and larger than 6 degrees (confined to a quadrant) in V3A. These estimates of RF sizes in human visual cortex are strikingly similar to those measured in physiological mapping studies in the homologous visual areas in monkeys.

A typical scene contains many different objects that, because of the limited processing capacity of the visual system, compete for neural representation. The competition among multiple objects in visual cortex can be biased by both bottom-up sensory-driven mechanisms and top-down influences, such as selective attention. Functional brain imaging studies reveal that, both in the absence and in the presence of visual stimulation, biasing signals due to selective attention can modulate neural activity in visual cortex in several ways. Although the competition among stimuli for representation is ultimately resolved within visual cortex, the source of top-down biasing signals derives from a network of areas in frontal and parietal cortex.

The segregation of visual scenes based on contour information is a fundamental process of early vision. Contours can be defined by simple cues, such as luminance, as well as by more complex cues, such as texture. Single-cell recording studies in monkeys suggest that the neural processing of complex contours starts as early as primary visual cortex. Additionally, lesion studies in monkeys indicate an important contribution of higher order areas to these processes. Using functional MRI, we have investigated the level at which neural correlates of texture segregation can be found in the human visual cortex. Activity evoked by line textures, with and without texture-defined boundaries, was compared in five healthy subjects. Areas V1, V2/VP, V4, TEO, and V3A were activated by both kinds of line textures as compared with blank presentations. Textures with boundaries forming a checkerboard pattern, relative to uniform textures, evoked significantly more activity in areas V4, TEO, less reliably in V3A, but not in V1 or V2/VP. These results provide evidence that higher order areas with large receptive fields play an important role in the segregation of visual scenes based on texture-defined boundaries.

Responses of striate neurons to line textures were investigated in anesthetized and paralyzed adult cats. Light bars centered over the excitatory receptive field (RF) were presented with different texture surrounds composed of many similar bars. In two test series, responses of 169 neurons to textures with orientation contrast (surrounding bars orthogonal to the center bar) or motion contrast (surrounding bars moving opposite to the center bar) were compared to the responses to the corresponding uniform texture conditions (all lines parallel, coherent motion) and to the center bar alone. In the majority of neurons center bar responses were suppressed by the texture surrounds. Two main effects were found. Some neurons were generally suppressed by either texture surround. Other neurons were less suppressed by texture displaying orientation or motion (i.e. feature) contrast than by the respective uniform texture, so that their responses to orientation or motion contrast appeared to be relatively enhanced (preference for feature contrast). General suppression was obtained in 33% of neurons tested for orientation and in 19% of neurons tested for motion. Preference for orientation or motion contrast was obtained in 22% and 34% of the neurons, respectively, and was also seen in the mean response of the population. One hundred nineteen neurons were studied in both orientation and motion tests. General suppression was correlated across the orientation and motion dimension, but not preference for feature contrast. We also distinguished modulatory effects from end-zones and flanks using butterfly-configured texture patterns. Both regions contributed to the generally suppressive effects. Preference for orientation or motion contrast was not generated from either end-zones or flanks exclusively. Neurons with preference for feature contrast may form the physiological basis of the perceptual saliency of pop-out elements in line textures. If so, pop-out of motion and pop-out of orientation would be encoded in different pools of neurons at the level of striate cortex.

When subjects direct attention to a particular location in a visual scene, responses in the visual cortex to stimuli presented at that location are enhanced, and the suppressive influences of nearby distractors are reduced. What is the top-down signal that modulates the response to an attended versus an unattended stimulus? Here, we demonstrate increased activity related to attention in the absence of visual stimulation in extrastriate cortex when subjects covertly directed attention to a peripheral location expecting the onset of visual stimuli. Frontal and parietal areas showed a stronger signal increase during this expectation than did visual areas. The increased activity in visual cortex in the absence of visual stimulation may reflect a top-down bias of neural signals in favor of the attended location, which derives from a fronto-parietal network.

Repetitive transcranial magnetic stimulation (rTMS) is a promising new treatment for patients with major depression. However, the mechanisms underlying the antidepressive action of rTMS are widely unclear. Rapid eye movement (REM) sleep has been shown to play an important role in the pathophysiology of depression. In the present study we demonstrate that rTMS delays the first REM sleep epoch on average by 17 min (102.6 +/-22.5 min vs 85.7+/-18.8 min; p < 0.02) and prolongs the nonREM-REM cycle length (109.1+/-11.4 min vs 101.8+/-13.2min, p< 0.012). These rTMS-induced changes in REM sleep variables correspond to findings observed after pharmacological and electroconvulsive treatment of depression. Therefore, it is likely that the capability of rTMS to affect circadian and ultradian biological rhythms contributes to its antidepressive action.

Transient visual field defects (VFDs) and phosphenes were induced in normal volunteers by means of transcranial magnetic stimulation (TMS) using a circular magnetic coil of 12.5 cm diameter placed with its lower rim 2-4 cm above the inion in the midline. Subjects had to detect small, bright dots presented randomly for 14 ms in one of 60 locations on a computer screen resulting in a plot of the central 9 degrees of the visual field. In 8 of 17 subjects, transient VFDs were inducible at peak magnetic field strenghts of 1.1-1.4 T. In the central 1-3 degrees, detection of targets was impaired in both the upper and lower visual field, whereas at 4-9 degrees large parts of only the lower visual field were affected with a sharp cut-off along the horizontal meridian. Targets at 1 degree in the lower field were affected with lower TMS intensities than corresponding locations in the upper or peripheral locations in the lower field. Detection of central targets was affected at more caudal stimulation sites than detection of peripheral targets. Phosphenes were elicitable in 14 of 17 subjects at clearly lower field strengths of 0.6-1.0 T. Many subjects perceived chromatophosphenes. From a discussion of the literature on patients with VFDs and the known topography of the human visual system, it is concluded that the transient VFDs at 1-3 degrees are probably due to stimulation of both striate cortex (V1) and extrastriate areas (V2/V3), while VFDs in the lower visual field at eccentricities 4-9 degrees are due to stimulation of V2/V3 but not V1.

A typical scene contains many different objects, but the capacity of the visual system to process multiple stimuli at a given time is limited. Thus, attentional mechanisms are required to select relevant objects from among the many objects competing for visual processing. Evidence from functional magnetic resonance imaging (MRI) in humans showed that when multiple stimuli are present simultaneously in the visual field, their cortical representations within the object recognition pathway interact in a competitive, suppressive fashion. Directing attention to one of the stimuli counteracts the suppressive influence of nearby stimuli. This mechanism may serve to filter out irrelevant information in cluttered visual scenes.

We propose a system for head fixation and neuronal recording that minimizes surgery for implantation. Fixation is obtained by posts which are attached to the opposite sides of the skull and are connected by a rigid frame around the animal's head. As forces are counterbalanced and distributed around the head, the system does not need to be implanted into the skull, and thus allows for continuous adjustment to the growing skull in young animals. Except for small incisions for the posts, the skin over the skull is left intact. Recording is achieved through small bone holes which are easily reached by means of conical guide tubes. The system provides perfect stability of recording, allows flexible access to various areas of the brain and can be easily removed during longer pauses in experiments. The use of this system may also decrease the number of laboratory animals needed.

We have recorded from extrastriate area V4 in monkeys performing a visual search task. When animals became tired or drowsy, responses to visual stimulation were often reduced or even completely blocked, and background activity changed to the burst-pause pattern typically seen in sleep. In spite of such neuronal sleep observed in V4, animals continued to perform the visual task, indicating that at least the primary visual cortex was still working. This observation shows that sleep does not develop simultaneously in all cortical areas but may affect some areas earlier than others. In particular conditions, local sleep of certain areas may be a stable and long-lasting phenomenon.

Neuronal responses to static and moving texture patterns were investigated in the striate cortex of anaesthetized and paralysed adults cats. Texture patterns were composed of a central light bar presented in the excitatory receptive field of a cell and an array of many similar elements in the surround. For the static condition, elements in the surround were either parallel or orthogonal to the centre line (orientation test). For the moving condition, centre and surround elements (all at same orientation) moved either in the same or in the opposite directions (motion test). Thirty-six percent (31/86) of the neurons tested for motion and 24% (24/99) of the neurons tested for orientation responded more strongly to the patterns displaying feature contrast than to the uniform patterns. These neurons may form a neural basis for visual pop-out of orientation and motion.

Coloured light surrounding a white surface of about equal luminance makes the white surface appear illuminated with an unsaturated light of the complementary colour. In an attempt to discover the neurophysiological basis of such colour induction, we recorded from spectrally opponent cells of the parvocellular layers of the lateral geniculate nucleus (P-LGN) of anaesthetized macaques. Only cells with wide-band (W) spectral sensitivity in the short (S) or long wavelength (L) part of the spectrum (WS, WL) are excited by white spots of light centred on their receptive field. Cells with narrow-band (N) spectral sensitivity (NS, NL) and light-inhibited (LI) cells are inhibited by white light. Therefore, it is likely that the code for white is contained in a balanced excitation of the W cells. The effects of continuous illumination of remote surrounds with different wavelengths on the responses to achromatic light stimuli were investigated. Responses [on minus maintained discharge rate (MDR) or on-minus-off] were determined for white spots (1 - 3 degrees diameter) flashed on the receptive field centre, presented either alone or in the presence of an annular surround of equal luminance (inner diameter 5 degrees; outer diameter 20 degrees ). During red surround illumination the responses of WL cells to white spots tended to be reduced as were those of WS cells during blue surround illumination. Surround illumination with the opponent colour had more variable effects, neither WS nor WL cells showing a significant alteration of their mean response to white during surround illumination with opponent light. Response alterations were to a large extent due to changes in MDR, which increased in WS cells during blue surround illumination and in WL cells during red surround illumination. It is argued that the surround effects on centre responses are due to intraocular stray light rather than lateral connections in the retina. The surround effects also depended to some extent on the size of the test spot. LI cells and the very rare parvocellular panchromatic on-cells showed no chromatic response changes during coloured surround illumination. Inasmuch as the excitation of WS cells, either alone or in combination with NS cell activation, is involved in coding for green and blue, and that of WL cells, in combination with NL cell activation, is involved in coding for red and yellow in perception, the shift of excitation towards one or the other W cell group indicates relatively more red or green signals in the white response, consistent with and in the same direction as colour induction. In addition, the summed population response of WS and WL cells is decreased during surround illumination with any colour including white. This is related to brightness decrease during surround illumination in perception.