Control of visuotemporal attention by inferior parietal and superior temporal cortex

The human cortical visual system is organized into major pathways: a dorsal stream projecting to the superior parietal lobe (SPL), considered to be critical for visuospatial perception or on-line control of visually guided movements, and a ventral stream leading to the inferotemporal cortex, mediating object perception. Between these structures lies a large region, consisting of the inferior parietal lobe (IPL) and superior temporal gyrus (STG), the function of which is controversial. Lesions here can lead to spatial neglect, a condition associated with abnormal visuospatial perception as well as impaired visually guided movements, suggesting that the IPL+STG may have largely a "dorsal" role. Here, we use a nonspatial task to examine the deployment of visuotemporal attention in focal lesion patients, with or without spatial neglect. We show that, regardless of the presence of neglect, damage to the IPL+STG leads to a more prolonged deployment of visuotemporal attention compared to lesions of the SPL. Our findings suggest that the human IPL+STG makes an important contribution to nonspatial perception, and this is consistent with a role that is neither strictly "dorsal" nor "ventral". We propose instead that the IPL+STG has a top-down control role, contributing to the functions of both dorsal and ventral visual systems.     

形状和空间位置知觉两条通路的功能磁共振研究

利用功能磁共振成像（ｆＭＲＩ） 技术,研究在处理形状知觉、位置知觉和特定形状图形的空间位置知觉的情况下,人类视皮层背侧（Ｄｏｒｓａｌ ｓｔｒｅａｍ） 和腹侧（Ｖｅｎｔｒａｌ ｓｔｒｅａｍ） 两条通路是怎样反应的。结果发现：形状知觉仅引起腹侧通路的兴奋;空间位置的知觉引起背侧通路的兴奋;特定形状的空间位置知觉引起腹侧通路和背侧通路的共同兴奋。这一结果丰富了对人类视觉皮层的两条通路在功能上定位的认识。     

An evolving view of duplex vision: separate but interacting cortical pathways for perception and action

In 1992, Goodale and Milner proposed a division of labour in the visual pathways of the primate cerebral cortex between a dorsal stream specialised for the visual control of action and a ventral stream dedicated to the perception of the visual world. In the years since this original proposal, support for the perception-action hypothesis has come from neuroimaging experiments, human neuropsychology, monkey neurophysiology, and human psychophysical experiments. Indeed, some of the strongest support for this hypothesis has come from behavioural experiments showing that visually guided actions are largely refractory to perceptual illusions. Although controversial, the findings from this literature both support the original hypothesis and suggest important modifications. The ongoing challenge for neurobiologists is to map these behavioural findings onto their corresponding neural substrates.     

Contributions of magno- and parvocellular channels to conscious and non-conscious vision

The dorsal and ventral cortical pathways, driven predominantly by magnocellular (M) and parvocellular (P) inputs, respectively, assume leading roles in models of visual information processing. Although in prior proposals, the dorsal and ventral pathways support non-conscious and conscious vision, respectively, recent modelling and empirical developments indicate that each pathway plays important roles in both non-conscious and conscious vision. In these models, the ventral P-pathway consists of one subpathway processing an object''s contour features, e.g. curvature, the other processing its surface attributes, e.g. colour. Masked priming studies have shown that feed-forward activity in the ventral P-pathway on its own supports non-conscious processing of contour and surface features. The dorsal M-pathway activity contributes directly to conscious vision of motion and indirectly to object vision by projecting to prefrontal cortex, which in turn injects top-down neural activity into the ventral P-pathway and there ‘ignites’ feed-forward–re-entrant loops deemed necessary for conscious vision. Moreover, an object''s shape or contour remains invisible without the prior conscious registration of its surface properties, which for that reason are taken to comprise fundamental visual qualia. Besides suggesting avenues for future research, these developments bear on several recent and past philosophical issues.     

Posterior Parietal Cortex Drives Inferotemporal Activations During Three-Dimensional Object Vision

The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-microstimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams.     

Top-down modulations from dorsal stream in lexical recognition: an effective connectivity FMRI study

Both the ventral and dorsal visual streams in the human brain are known to be involved in reading. However, the interaction of these two pathways and their responses to different cognitive demands remains unclear. In this study, activation of neural pathways during Chinese character reading was acquired by using a functional magnetic resonance imaging (fMRI) technique. Visual-spatial analysis (mediated by the dorsal pathway) was disassociated from lexical recognition (mediated by the ventral pathway) via a spatial-based lexical decision task and effective connectivity analysis. Connectivity results revealed that, during spatial processing, the left superior parietal lobule (SPL) positively modulated the left fusiform gyrus (FG), while during lexical processing, the left SPL received positive modulatory input from the left inferior frontal gyrus (IFG) and sent negative modulatory output to the left FG. These findings suggest that the dorsal stream is highly involved in lexical recognition and acts as a top-down modulator for lexical processing.     

Dissociation between ventral and dorsal fMRI activation during object and action recognition

Neuropsychological case studies suggest the existence of two functionally separate visual streams: the ventral pathway, central for object recognition; and the dorsal pathway, engaged in visually guided actions. However, a clear dissociation between the functions of the two streams has not been decisively shown in intact humans. In this study, we demonstrate dissociation between dorsal and ventral fMRI activation patterns during observation of object manipulation video clips. Parietal areas, such as anterior intraparietal sulcus (aIPS) display grasp viewing-dependent adaptation (i.e., fMR adaptation during repeated viewing of the same object-grasping movement) as well as a contralateral preference for the viewed manipulating hand. Ventral regions, such as the fusiform gyrus, show similar characteristics (i.e., adaptation, contralateral preference), but these depend on object identity. Our results support the hypothesized functional specialization in the visual system and suggest that parietal areas (such as aIPS) are engaged in action recognition, as well as in action planning.     

Cerebral Activations Related to Writing and Drawing with Each Hand

BackgroundWriting is a sequential motor action based on sensorimotor integration in visuospatial and linguistic functional domains. To test the hypothesis of lateralized circuitry concerning spatial and language components involved in such action, we employed an fMRI paradigm including writing and drawing with each hand. In this way, writing-related contributions of dorsal and ventral premotor regions in each hemisphere were assessed, together with effects in wider distributed circuitry. Given a right-hemisphere dominance for spatial action, right dorsal premotor cortex dominance was expected in left-hand writing while dominance of the left ventral premotor cortex was expected during right-hand writing.MethodsSixteen healthy right-handed subjects were scanned during audition-guided writing of short sentences and simple figure drawing without visual feedback. Tapping with a pencil served as a basic control task for the two higher-order motor conditions. Activation differences were assessed with Statistical Parametric Mapping (SPM).ResultsWriting and drawing showed parietal-premotor and posterior inferior temporal activations in both hemispheres when compared to tapping. Drawing activations were rather symmetrical for each hand. Activations in left- and right-hand writing were left-hemisphere dominant, while right dorsal premotor activation only occurred in left-hand writing, supporting a spatial motor contribution of particularly the right hemisphere. Writing contrasted to drawing revealed left-sided activations in the dorsal and ventral premotor cortex, Broca’s area, pre-Supplementary Motor Area and posterior middle and inferior temporal gyri, without parietal activation.DiscussionThe audition-driven postero-inferior temporal activations indicated retrieval of virtual visual form characteristics in writing and drawing, with additional activation concerning word form in the left hemisphere. Similar parietal processing in writing and drawing pointed at a common mechanism by which such visually formatted information is used for subsequent sensorimotor integration along a dorsal visuomotor pathway. In this, the left posterior middle temporal gyrus subserves phonological-orthographical conversion, dissociating dorsal parietal-premotor circuitry from perisylvian circuitry including Broca''s area.     

Differential effects of viewpoint on object-driven activation in dorsal and ventral streams

Using fMRI, we showed that an area in the ventral temporo-occipital cortex (area vTO), which is part of the human homolog of the ventral stream of visual processing, exhibited priming for both identical and depth-rotated images of objects. This pattern of activation in area vTO corresponded to performance in a behavioral matching task. An area in the caudal part of the intraparietal sulcus (area cIPS) also showed priming, but only with identical images of objects. This dorsal-stream area treated rotated images as new objects. The difference in the pattern of priming-related activation in the two areas may reflect the respective roles of the ventral and dorsal streams in object recognition and object-directed action.     

Sexual dimorphism in the visual system of flies: The divided brain of male Bibionidae (Diptera)

Summary The mapping of the compound eyes onto the visual neuropils and the cell types in the lamina and the lobula complex of Bibionidae (Diptera) were studied by means of extracellular cobalt injections and Golgi impregnations. Dorsal and ventral eyes in males map into separate dorsal-and ventral neuropils up to the level of the lobula complex. The dorsal-eye lamina is unilayered, while the ventral-eye lamina in males and the lamina in females are multilayered: layers A and C are invaded by en-passant terminals of long visual fibres, layer B by the terminals of short visual fibres. Long visual fibres have a short and a long terminal in the ventral medulla with terminal specialisations in three distinct layers. Only one type of receptor ending exists in the dorsal medulla, the terminal branches of which are restricted to one layer only. Arrays of contralateral neurones are found in the medial part of the dorsal lobula, which receives input from the zone of binocular vision of the ipsilateral dorsal eye, and in the posterior dorsal lobula and lobula plate. The dorsal lobula plate contains large tangential neurones, the dendritic arborisations of which are revealed by cobalt injection into the thoracic ganglia. The divided brain of male bibionids offers the opportunity to investigate separately the nervous systems involved in sex-specific visually guided flight behaviour and in general visually guided flight control.     

Is visual processing in the dorsal stream accessible to consciousness?

There are two highly interconnected clusters of visually responsive areas in the primate cortex. These two clusters have relatively few interconnections with each other, though those interconnections are undoubtedly important. One of the two main clusters (the dorsal stream) links the primary visual cortex (V1) to superior regions of the occipito-parietal cortex, while the other (the ventral stream) links V1 to inferior regions of the occipito-temporal cortex. According to our current understanding of the functional anatomy of these two systems, the dorsal stream's principal role is to provide real-time 'bottom-up' visual guidance of our movements online. In contrast, the ventral stream, in conjunction with top-down information from visual and semantic memory, provides perceptual representations that can serve recognition, visual thought, planning and memory offline. In recent years, this interpretation, initially based chiefly on studies of non-human primates and human neurological patients, has been well supported by functional MRI studies in humans. This perspective presents empirical evidence for the contention that the dorsal stream governs the visual control of movement without the intervention of visual awareness.     

The Role of Parieto-Occipital Junction in the Interaction between Dorsal and Ventral Streams in Disparity-Defined Near and Far Space Processing

Neuropsychological and functional MRI data suggest that two functionally and anatomically dissociable streams of visual processing exist: a ventral perception-related stream and a dorsal action-related stream. However, relatively little is known about how the two streams interact in the intact brain during the production of adaptive behavior. Using functional MRI and a virtual three-dimensional paradigm, we aimed at examining whether the parieto-occipital junction (POJ) acts as an interface for the integration and processing of information between the dorsal and ventral streams in the near and far space processing. Virtual reality three-dimensional near and far space was defined by manipulating binocular disparity, with -68.76 arcmin crossed disparity for near space and +68.76 arcmin uncrossed disparity for near space. Our results showed that the POJ and bilateral superior occipital gyrus (SOG) showed relative increased activity when responded to targets presented in the near space than in the far space, which was independent of the retinotopic and perceived sizes of target. Furthermore, the POJ showed the enhanced functional connectivity with both the dorsal and ventral streams during the far space processing irrespective of target sizes, supporting that the POJ acts as an interface between the dorsal and ventral streams in disparity-defined near and far space processing. In contrast, the bilateral SOG showed the enhanced functional connectivity only with the ventral stream if retinotopic sizes of targets in the near and far spaces were matched, which suggested there was a functional dissociation between the POJ and bilateral SOG.     

Functional specialization of seven mouse visual cortical areas

To establish the mouse as a genetically tractable model for high-order visual processing, we characterized fine-scale retinotopic organization of visual cortex and determined functional specialization of layer 2/3 neuronal populations in seven retinotopically identified areas. Each area contains a distinct visuotopic representation and encodes a unique combination of spatiotemporal features. Areas LM, AL, RL, and AM prefer up to three times faster temporal frequencies and significantly lower spatial frequencies than V1, while V1 and PM prefer high spatial and low temporal frequencies. LI prefers both high spatial and temporal frequencies. All extrastriate areas except LI increase orientation selectivity compared to V1, and three areas are significantly more direction selective (AL, RL, and AM). Specific combinations of spatiotemporal representations further distinguish areas. These results reveal that mouse higher visual areas are functionally distinct, and separate groups of areas may be specialized for motion-related versus pattern-related computations, perhaps forming pathways analogous to dorsal and ventral streams in other species.     

Spatial modulation of primate inferotemporal responses by eye position

Background

A key aspect of representations for object recognition and scene analysis in the ventral visual stream is the spatial frame of reference, be it a viewer-centered, object-centered, or scene-based coordinate system. Coordinate transforms from retinocentric space to other reference frames involve combining neural visual responses with extraretinal postural information.

Methodology/Principal Findings

We examined whether such spatial information is available to anterior inferotemporal (AIT) neurons in the macaque monkey by measuring the effect of eye position on responses to a set of simple 2D shapes. We report, for the first time, a significant eye position effect in over 40% of recorded neurons with small gaze angle shifts from central fixation. Although eye position modulates responses, it does not change shape selectivity.

Conclusions/Significance

These data demonstrate that spatial information is available in AIT for the representation of objects and scenes within a non-retinocentric frame of reference. More generally, the availability of spatial information in AIT calls into questions the classic dichotomy in visual processing that associates object shape processing with ventral structures such as AIT but places spatial processing in a separate anatomical stream projecting to dorsal structures.     

Visual perception skills: a comparison between patients with Noonan syndrome and 22q11.2 deletion syndrome

Ventral and dorsal streams are visual pathways deputed to transmit information from the photoreceptors of the retina to the lateral geniculate nucleus and then to the primary visual cortex (V1). Several studies investigated whether one pathway is more vulnerable than the other during development, and whether these streams develop at different rates. The results are still discordant. The aim of the present study was to understand the functionality of the dorsal and the ventral streams in two populations affected by different genetic disorders, Noonan syndrome (NS) and 22q11.2 deletion syndrome (22q11.2DS), and explore the possible genotype–phenotype relationships. ‘Form coherence’ abilities for the ventral stream and ‘motion coherence’ abilities for the dorsal stream were evaluated in 19 participants with NS and 20 participants with 22q11.2DS. Collected data were compared with 55 age‐matched controls. Participants with NS and 22q11.2DS did not differ in the form coherence task, and their performance was significantly lower than that of controls. However, in the motion coherence task, the group with NS and controls did not differ, and both obtained significantly higher scores than the group with 22q11.2DS. Our findings indicate that deficits in the dorsal stream are related to the specific genotype, and that in our syndromic groups the ventral stream is more vulnerable than the dorsal stream.     

Cerebral Activations Related to Audition-Driven Performance Imagery in Professional Musicians

Functional Magnetic Resonance Imaging (fMRI) was used to study the activation of cerebral motor networks during auditory perception of music in professional keyboard musicians (n = 12). The activation paradigm implied that subjects listened to two-part polyphonic music, while either critically appraising the performance or imagining they were performing themselves. Two-part polyphonic audition and bimanual motor imagery circumvented a hemisphere bias associated with the convention of playing the melody with the right hand. Both tasks activated ventral premotor and auditory cortices, bilaterally, and the right anterior parietal cortex, when contrasted to 12 musically unskilled controls. Although left ventral premotor activation was increased during imagery (compared to judgment), bilateral dorsal premotor and right posterior-superior parietal activations were quite unique to motor imagery. The latter suggests that musicians not only recruited their manual motor repertoire but also performed a spatial transformation from the vertically perceived pitch axis (high and low sound) to the horizontal axis of the keyboard. Imagery-specific activations in controls were seen in left dorsal parietal-premotor and supplementary motor cortices. Although these activations were less strong compared to musicians, this overlapping distribution indicated the recruitment of a general ‘mirror-neuron’ circuitry. These two levels of sensori-motor transformations point towards common principles by which the brain organizes audition-driven music performance and visually guided task performance.     

Two Speed Factors of Visual Recognition Independently Correlated with Fluid Intelligence

Growing evidence indicates a moderate but significant relationship between processing speed in visuo-cognitive tasks and general intelligence. On the other hand, findings from neuroscience proposed that the primate visual system consists of two major pathways, the ventral pathway for objects recognition and the dorsal pathway for spatial processing and attentive analysis. Previous studies seeking for visuo-cognitive factors of human intelligence indicated a significant correlation between fluid intelligence and the inspection time (IT), an index for a speed of object recognition performed in the ventral pathway. We thus presently examined a possibility that neural processing speed in the dorsal pathway also represented a factor of intelligence. Specifically, we used the mental rotation (MR) task, a popular psychometric measure for mental speed of spatial processing in the dorsal pathway. We found that the speed of MR was significantly correlated with intelligence scores, while it had no correlation with one’s IT (recognition speed of visual objects). Our results support the new possibility that intelligence could be explained by two types of mental speed, one related to object recognition (IT) and another for manipulation of mental images (MR).     

A stimulus-driven approach to object identity and location processing in the human brain

The primate visual system is considered to be segregated into ventral and dorsal streams specialized for processing object identity and location, respectively. We reexamined the dorsal/ventral model using a stimulus-driven approach to object identity and location processing. While looking at repeated presentations of a standard object at a standard location, subjects monitored for any infrequent "oddball" changes in object identity, location, or identity and location (conjunction). While the identity and location oddballs preferentially activated ventral and dorsal brain regions respectively, each oddball type activated both pathways. Furthermore, all oddball types recruited the lateral temporal cortex and the temporo-parietal junction. These findings suggest that a strict dorsal/ventral dual-stream model does not fully account for the perception of novel objects in space.     

Evolution and Optimality of Similar Neural Mechanisms for Perception and Action during Search

A prevailing theory proposes that the brain''s two visual pathways, the ventral and dorsal, lead to differing visual processing and world representations for conscious perception than those for action. Others have claimed that perception and action share much of their visual processing. But which of these two neural architectures is favored by evolution? Successful visual search is life-critical and here we investigate the evolution and optimality of neural mechanisms mediating perception and eye movement actions for visual search in natural images. We implement an approximation to the ideal Bayesian searcher with two separate processing streams, one controlling the eye movements and the other stream determining the perceptual search decisions. We virtually evolved the neural mechanisms of the searchers'' two separate pathways built from linear combinations of primary visual cortex receptive fields (V1) by making the simulated individuals'' probability of survival depend on the perceptual accuracy finding targets in cluttered backgrounds. We find that for a variety of targets, backgrounds, and dependence of target detectability on retinal eccentricity, the mechanisms of the searchers'' two processing streams converge to similar representations showing that mismatches in the mechanisms for perception and eye movements lead to suboptimal search. Three exceptions which resulted in partial or no convergence were a case of an organism for which the targets are equally detectable across the retina, an organism with sufficient time to foveate all possible target locations, and a strict two-pathway model with no interconnections and differential pre-filtering based on parvocellular and magnocellular lateral geniculate cell properties. Thus, similar neural mechanisms for perception and eye movement actions during search are optimal and should be expected from the effects of natural selection on an organism with limited time to search for food that is not equi-detectable across its retina and interconnected perception and action neural pathways.     

Is Attention Based on Spatial Contextual Memory Preferentially Guided by Low Spatial Frequency Signals?

A popular model of visual perception states that coarse information (carried by low spatial frequencies) along the dorsal stream is rapidly transmitted to prefrontal and medial temporal areas, activating contextual information from memory, which can in turn constrain detailed input carried by high spatial frequencies arriving at a slower rate along the ventral visual stream, thus facilitating the processing of ambiguous visual stimuli. We were interested in testing whether this model contributes to memory-guided orienting of attention. In particular, we asked whether global, low-spatial frequency (LSF) inputs play a dominant role in triggering contextual memories in order to facilitate the processing of the upcoming target stimulus. We explored this question over four experiments. The first experiment replicated the LSF advantage reported in perceptual discrimination tasks by showing that participants were faster and more accurate at matching a low spatial frequency version of a scene, compared to a high spatial frequency version, to its original counterpart in a forced-choice task. The subsequent three experiments tested the relative contributions of low versus high spatial frequencies during memory-guided covert spatial attention orienting tasks. Replicating the effects of memory-guided attention, pre-exposure to scenes associated with specific spatial memories for target locations (memory cues) led to higher perceptual discrimination and faster response times to identify targets embedded in the scenes. However, either high or low spatial frequency cues were equally effective; LSF signals did not selectively or preferentially contribute to the memory-driven attention benefits to performance. Our results challenge a generalized model that LSFs activate contextual memories, which in turn bias attention and facilitate perception.