The primate visual system contains two major cortical pathways: a ventral-temporal pathway that has been associated with object processing and recognition, and a dorsal-parietal pathway that has been associated with spatial processing and action guidance. Our understanding of the role of the dorsal pathway, in particular, has greatly evolved within the framework of the two-pathway hypothesis since its original conception. Here, we present a comparative review of the primate dorsal pathway in humans and monkeys based on electrophysiological, neuroimaging, neuropsychological, and neuroanatomical studies. We consider similarities and differences across species in terms of the topographic representation of visual space; specificity for eye, reaching, or grasping movements; multi-modal response properties; and the representation of objects and tools. We also review the relative anatomical location of functionally- and topographically-defined regions of the posterior parietal cortex. An emerging theme from this comparative analysis is that non-spatial information is represented to a greater degree, and with increased complexity, in the human dorsal visual system. We propose that non-spatial information in the primate parietal cortex contributes to the perception-to-action system aimed at manipulating objects in peripersonal space. In humans, this network has expanded in multiple ways, including the development of a dorsal object vision system mirroring the complexity of the ventral stream, the integration of object information with parietal working memory systems, and the emergence of tool-specific object representations in the anterior intraparietal sulcus and regions of the inferior parietal lobe. We propose that these evolutionary changes have enabled the emergence of human-specific behaviors, such as the sophisticated use of tools.
Frontiers for Young Minds puts kids in charge of scientific publications by having them control the review process. This provides kids the ability to shape the way science is taught and to better understand the scientific method.
Unraveling how brain regions communicate is crucial for understanding how the brain processes external and internal information. Neuronal oscillations within and across brain regions have been proposed to play a crucial role in this process. Two main hypotheses have been suggested for routing of information based on oscillations, namely communication through coherence and gating by inhibition. Here, we propose a framework unifying these two hypotheses that is based on recent empirical findings. We discuss a theory in which communication between two regions is established by phase synchronization of oscillations at lower frequencies (<25 Hz), which serve as temporal reference frame for information carried by high-frequency activity (>40 Hz). Our framework, consistent with numerous recent empirical findings, posits that cross-frequency interactions are essential for understanding how large-scale cognitive and perceptual networks operate.
Recent findings in the visual system of nonhuman primates have demonstrated an important role of gamma-band activity (40-100 Hz) in the feedforward flow of sensory information, whereas feedback control appears to be established dynamically by oscillations in the alpha (8-13 Hz) and beta (13-18 Hz) bands (van Kerkoerle et al., 2014; Bastos et al., 2015). It is not clear, however, how alpha oscillations are controlled and how they interact with the flow of visual information mediated by gamma-band activity. Using noninvasive human MEG recordings in subjects performing a visuospatial attention task, we show that fluctuations in alpha power during a delay period in a spatial attention task preceded subsequent stimulus-driven gamma-band activity. Importantly, these interactions correlated with behavioral performance. Using Granger analysis, we further show that the right frontal-eye field (rFEF) exerted feedback control of the visual alpha oscillations. Our findings suggest that alpha oscillations controlled by the FEF route cortical information flow by modulating gamma-band activity.SIGNIFICANCE STATEMENT Visual perception relies on a feedforward flow of information from sensory regions, which is modulated by a feedback drive. We have identified the neuronal dynamics supporting integration of the feedforward and feedback information. Alpha oscillations in early visual regions reflect feedback control when spatial attention is allocated and this control is exercised by the right frontal eye field. Importantly, the alpha-band activity predicted both performance and activity in the gamma band. In particular, gamma activity was modulated by the phase of the alpha oscillations. These findings provide novel insight into how the brain operates as a network and suggest that the integration of feedforward and feedback information is implemented by cross-frequency interactions between slow and fast neuronal oscillations.
Visual integration dysfunction characterizes schizophrenia, but prior studies have not yet established whether the problem arises by the first psychotic episode or worsens with illness duration. To investigate the issue, we compared chronic schizophrenia patients (SZs), first episode psychosis patients (FEs), and well-matched healthy controls on a brief but sensitive psychophysical task in which subjects attempted to locate an integrated shape embedded in noise. Task difficulty depended on the number of noise elements co-presented with the shape. For half of the experiment, the entire display was scaled down in size to produce a high spatial frequency (HSF) condition, which has been shown to worsen patient integration deficits. Catch trials-in which the circular target appeared without noise-were also added so as to confirm that subjects were paying adequate attention. We found that controls integrated contours under noisier conditions than FEs, who, in turn, integrated better than SZs. These differences, which were at times large in magnitude (d = 1.7), clearly emerged only for HSF displays. Catch trial accuracy was above 95% for each group and could not explain the foregoing differences. Prolonged illness duration predicted poorer HSF integration across patients, but age had little effect on controls, indicating that the former factor was driving the effect in patients. Taken together, a brief psychophysical task efficiently demonstrates large visual integration impairments in schizophrenia. The deficit arises by the first psychotic episode, worsens with illness duration, and may serve as a biomarker of illness progression. (PsycINFO Database Record
The human visual system contains an array of topographically organized regions. Identifying these regions in individual subjects is a powerful approach to group-level statistical analysis, but this is not always feasible. We addressed this limitation by generating probabilistic maps of visual topographic areas in 2 standardized spaces suitable for use with adult human brains. Using standard fMRI paradigms, we identified 25 topographic maps in a large population of individual subjects (N = 53) and transformed them into either a surface- or volume-based standardized space. Here, we provide a quantitative characterization of the inter-subject variability within and across visual regions, including the likelihood that a given point would be classified as a part of any region (full probability map) and the most probable region for any given point (maximum probability map). By evaluating the topographic organization across the whole of visual cortex, we provide new information about the organization of individual visual field maps and large-scale biases in visual field coverage. Finally, we validate each atlas for use with independent subjects. Overall, the probabilistic atlases quantify the variability of topographic representations in human cortex and provide a useful reference for comparing data across studies that can be transformed into these standard spaces.
Looking for objects in cluttered natural environments is a frequent task in everyday life. This process can be difficult, because the features, locations, and times of appearance of relevant objects often are not known in advance. Thus, a mechanism by which attention is automatically biased toward information that is potentially relevant may be helpful. We tested for such a mechanism across five experiments by engaging participants in real-world visual search and then assessing attentional capture for information that was related to the search set but was otherwise irrelevant. Isolated objects captured attention while preparing to search for objects from the same category embedded in a scene, as revealed by lower detection performance (Experiment 1A). This capture effect was driven by a central processing bottleneck rather than the withdrawal of spatial attention (Experiment 1B), occurred automatically even in a secondary task (Experiment 2A), and reflected enhancement of matching information rather than suppression of nonmatching information (Experiment 2B). Finally, attentional capture extended to objects that were semantically associated with the target category (Experiment 3). We conclude that attention is efficiently drawn towards a wide range of information that may be relevant for an upcoming real-world visual search. This mechanism may be adaptive, allowing us to find information useful for our behavioral goals in the face of uncertainty.
Human frontoparietal cortex has long been implicated as a source of attentional control. However, the mechanistic underpinnings of these control functions have remained elusive due to limitations of neuroimaging techniques that rely on anatomical landmarks to localize patterns of activation. The recent advent of topographic mapping via functional magnetic resonance imaging (fMRI) has allowed the reliable parcellation of the network into 18 independent subregions in individual subjects, thereby offering unprecedented opportunities to address a wide range of empirical questions as to how mechanisms of control operate. Here, we review the human neuroimaging literature that has begun to explore space-based, feature-based, object-based and category-based attentional control within the context of topographically defined frontoparietal cortex.
The human visual system can be divided into over two-dozen distinct areas, each of which contains a topographic map of the visual field. A fundamental question in vision neuroscience is how the visual system integrates information from the environment across different areas. Using neuroimaging, we investigated the spatial pattern of correlated BOLD signal across eight visual areas on data collected during rest conditions and during naturalistic movie viewing. The correlation pattern between areas reflected the underlying receptive field organization with higher correlations between cortical sites containing overlapping representations of visual space. In addition, the correlation pattern reflected the underlying widespread eccentricity organization of visual cortex, in which the highest correlations were observed for cortical sites with iso-eccentricity representations including regions with non-overlapping representations of visual space. This eccentricity-based correlation pattern appears to be part of an intrinsic functional architecture that supports the integration of information across functionally specialized visual areas.
UNLABELLED: The pulvinar is the largest nucleus in the primate thalamus and contains extensive, reciprocal connections with visual cortex. Although the anatomical and functional organization of the pulvinar has been extensively studied in old and new world monkeys, little is known about the organization of the human pulvinar. Using high-resolution functional magnetic resonance imaging at 3 T, we identified two visual field maps within the ventral pulvinar, referred to as vPul1 and vPul2. Both maps contain an inversion of contralateral visual space with the upper visual field represented ventrally and the lower visual field represented dorsally. vPul1 and vPul2 border each other at the vertical meridian and share a representation of foveal space with iso-eccentricity lines extending across areal borders. Additional, coarse representations of contralateral visual space were identified within ventral medial and dorsal lateral portions of the pulvinar. Connectivity analyses on functional and diffusion imaging data revealed a strong distinction in thalamocortical connectivity between the dorsal and ventral pulvinar. The two maps in the ventral pulvinar were most strongly connected with early and extrastriate visual areas. Given the shared eccentricity representation and similarity in cortical connectivity, we propose that these two maps form a distinct visual field map cluster and perform related functions. The dorsal pulvinar was most strongly connected with parietal and frontal areas. The functional and anatomical organization observed within the human pulvinar was similar to the organization of the pulvinar in other primate species.
SIGNIFICANCE STATEMENT: The anatomical organization and basic response properties of the visual pulvinar have been extensively studied in nonhuman primates. Yet, relatively little is known about the functional and anatomical organization of the human pulvinar. Using neuroimaging, we found multiple representations of visual space within the ventral human pulvinar and extensive topographically organized connectivity with visual cortex. This organization is similar to other nonhuman primates and provides additional support that the general organization of the pulvinar is consistent across the primate phylogenetic tree. These results suggest that the human pulvinar, like other primates, is well positioned to regulate corticocortical communication.
The brain has a limited capacity and therefore needs mechanisms to selectively enhance the information most relevant to one's current behavior. We refer to these mechanisms as "attention." Attention acts by increasing the strength of selected neural representations and preferentially routing them through the brain's large-scale network. This is a critical component of cognition and therefore has been a central topic in cognitive neuroscience. Here we review a diverse literature that has studied attention at the level of behavior, networks, circuits, and neurons. We then integrate these disparate results into a unified theory of attention.
UNLABELLED: Developmental topographic disorientation (DTD) is a life-long condition in which affected individuals are severely impaired in navigating around their environment. Individuals with DTD have no apparent structural brain damage on conventional imaging and the neural mechanisms underlying DTD are currently unknown. Using functional and diffusion tensor imaging, we present a comprehensive neuroimaging study of an individual, J.N., with well defined DTD. J.N. has intact scene-selective responses in the parahippocampal place area (PPA), transverse occipital sulcus, and retrosplenial cortex (RSC), key regions associated with scene perception and navigation. However, detailed fMRI studies probing selective tuning properties of these regions, as well as functional connectivity, suggest that J.N.'s RSC has an atypical response profile and an atypical functional coupling to PPA compared with human controls. This deviant functional profile of RSC is not due to compromised structural connectivity. This comprehensive examination suggests that the RSC may play a key role in navigation-related processing and that an alteration of the RSC's functional properties may serve as the neural basis for DTD.
SIGNIFICANCE STATEMENT: Individuals with developmental topographic disorientation (DTD) have a life-long impairment in spatial navigation in the absence of brain damage, neurological conditions, or basic perceptual or memory deficits. Although progress has been made in identifying brain regions that subserve normal navigation, the neural basis of DTD is unknown. Using functional and structural neuroimaging and detailed statistical analyses, we investigated the brain regions typically involved in navigation and scene processing in a representative DTD individual, J.N. Although scene-selective regions were identified, closer scrutiny indicated that these areas, specifically the retrosplenial cortex (RSC), were functionally disrupted in J.N. This comprehensive examination of a representative DTD individual provides insight into the neural basis of DTD and the role of the RSC in navigation-related processing.
Areas V3 and V4 are commonly thought of as individual entities in the primate visual system, based on definition criteria such as their representation of visual space, connectivity, functional response properties, and relative anatomical location in cortex. Yet, large-scale functional and anatomical organization patterns not only emphasize distinctions within each area, but also links across visual cortex. Specifically, the visuotopic organization of V3 and V4 appears to be part of a larger, supra-areal organization, clustering these areas with early visual areas V1 and V2. In addition, connectivity patterns across visual cortex appear to vary within these areas as a function of their supra-areal eccentricity organization. This complicates the traditional view of these regions as individual functional "areas." Here, we will review the criteria for defining areas V3 and V4 and will discuss functional and anatomical studies in humans and monkeys that emphasize the integration of individual visual areas into broad, supra-areal clusters that work in concert for a common computational goal. Specifically, we propose that the visuotopic organization of V3 and V4, which provides the criteria for differentiating these areas, also unifies these areas into the supra-areal organization of early visual cortex. We propose that V3 and V4 play a critical role in this supra-areal organization by filtering information about the visual environment along parallel pathways across higher-order cortex.
The efficient selection of behaviorally relevant objects from cluttered environments supports our everyday goals. Attentional selection has typically been studied in search tasks involving artificial and simplified displays. Although these studies have revealed important basic principles of attention, they do not explain how the brain efficiently selects familiar objects in complex and meaningful real-world scenes. Findings from recent neuroimaging studies indicate that real-world search is mediated by 'what' and 'where' attentional templates that are implemented in high-level visual cortex. These templates represent target-diagnostic properties and likely target locations, respectively, and are shaped by object familiarity, scene context, and memory. We propose a framework for real-world search that incorporates these recent findings and specifies directions for future study.
The Fifth International Workshop on Advances in Electrocorticography convened in San Diego, CA, on November 7-8, 2013. Advancements in methodology, implementation, and commercialization across both research and in the interval year since the last workshop were the focus of the gathering. Electrocorticography (ECoG) is now firmly established as a preferred signal source for advanced research in functional, cognitive, and neuroprosthetic domains. Published output in ECoG fields has increased tenfold in the past decade. These proceedings attempt to summarize the state of the art.
Schizophrenia patients poorly perceive Kanizsa figures and integrate co-aligned contour elements (Gabors). They also poorly process low spatial frequencies (SFs), which presumably reflects dysfunction along the dorsal pathway. Can contour grouping deficits be explained in terms of the spatial frequency content of the display elements? To address the question, we tested patients and matched controls on three contour grouping paradigms in which the SF composition was modulated. In the Kanizsa task, subjects discriminated quartets of sectored circles ("pac-men") that either formed or did not form Kanizsa shapes (illusory and fragmented conditions, respectively). In contour integration, subjects identified the screen quadrant thought to contain a closed chain of co-circular Gabors. In collinear facilitation, subjects attempted to detect a central low-contrast element flanked by collinear or orthogonal high-contrast elements, and facilitation corresponded to the amount by which collinear flankers reduced contrast thresholds. We varied SF by modifying the element features in the Kanizsa task and by scaling the entire stimulus display in the remaining tasks (SFs ranging from 4 to 12 cycles/deg). Irrespective of SF, patients were worse at discriminating illusory, but not fragmented shapes. Contrary to our hypothesis, collinear facilitation and contour integration were abnormal in the clinical group only for the higher SF (>=10 c/deg). Grouping performance correlated with clinical variables, such as conceptual disorganization, general symptoms, and levels of functioning. In schizophrenia, three forms of contour grouping impairments prominently arise and cannot be attributed to poor low SF processing. Neurobiological and clinical implications are discussed.
Using functional MRI (fMRI) and a sophisticated forward encoding and decoding approach across the cortical surface, a new study examines how attention alternates tuning functions across a large set of semantic categories. The results suggest a dynamic attention mechanism that allocates greater resources to the attended and related semantic categories at the expense of unattended ones.
The dorsal frontoparietal attention network has been subdivided into at least eight areas in humans. However, the circuitry linking these areas and the functions of different circuit paths remain unclear. Using a combination of neuroimaging techniques to map spatial representations in frontoparietal areas, their functional interactions, and structural connections, we demonstrate different pathways across human dorsal frontoparietal cortex for the control of spatial attention. Our results are consistent with these pathways computing object-centered and/or viewer-centered representations of attentional priorities depending on task requirements. Our findings provide an organizing principle for the frontoparietal attention network, where distinct pathways between frontal and parietal regions contribute to multiple spatial representations, enabling flexible selection of behaviorally relevant information.
The act of reaching to grasp an object requires the coordination between transporting the arm and shaping the hand. Neurophysiological, neuroimaging, neuroanatomic, and neuropsychological studies in macaque monkeys and humans suggest that the neural networks underlying grasping and reaching acts are at least partially separable within the posterior parietal cortex (PPC). To better understand how these neural networks have evolved in primates, we characterized the relationship between grasping- and reaching-related responses and topographically organized areas of the human intraparietal sulcus (IPS) using functional MRI. Grasping-specific activation was localized to the left anterior IPS, partially overlapping with the most anterior topographic regions and extending into the postcentral sulcus. Reaching-specific activation was localized to the left precuneus and superior parietal lobule, partially overlapping with the medial aspects of the more posterior topographic regions. Although the majority of activity within the topographic regions of the IPS was nonspecific with respect to movement type, we found evidence for a functional gradient of specificity for reaching and grasping movements spanning posterior-medial to anterior-lateral PPC. In contrast to the macaque monkey, grasp- and reach-specific activations were largely located outside of the human IPS.