Motion opponency examined throughout visual cortex with multivariate pattern analysis of fMRI data.

This study explores how the human brain solves the challenge of flicker noise in motion processing. Despite providing no useful directional motion information, flicker is common in the visual environment and exhibits omnidirectional motion energy which is processed by low-level motion detectors. Models of motion processing propose a mechanism called motion opponency that reduces flicker processing. Motion opponency involves the pooling of local motion signals to calculate an overall motion direction. A neural correlate of motion opponency has been observed in human area MT+/V5, whereby stimuli with perfectly balanced motion energy constructed from dots moving in counter-phase elicit a weaker response than nonbalanced (in-phase) motion stimuli. Building on this previous work, we used multivariate pattern analysis to examine whether the activation patterns elicited by motion opponent stimuli resemble that elicited by flicker noise across the human visual cortex. Robust multivariate signatures of opponency were observed in V5 and in V3A. Our results support the notion that V5 is centrally involved in motion opponency and in the reduction of flicker. Furthermore, these results demonstrate the utility of multivariate analysis methods in revealing the role of additional visual areas, such as V3A, in opponency and in motion processing more generally.

Differential processing of the direction and focus of expansion of optic flow stimuli in areas MST and V3A of the human visual cortex.

Human neuropsychological and neuroimaging studies have raised the possibility that different attributes of optic flow stimuli, namely radial direction and the position of the focus of expansion (FOE), are processed within separate cortical areas. In the human brain, visual areas V5/MT+ and V3A have been proposed as integral to the analysis of these different attributes of optic flow stimuli. To establish direct causal relationships between neural activity in human (h)V5/MT+ and V3A and the perception of radial motion direction and FOE position, we used transcranial magnetic stimulation (TMS) to disrupt cortical activity in these areas while participants performed behavioral tasks dependent on these different aspects of optic flow stimuli. The cortical regions of interest were identified in seven human participants using standard functional MRI retinotopic mapping techniques and functional localizers. TMS to area V3A was found to disrupt FOE positional judgments but not radial direction discrimination, whereas the application of TMS to an anterior subdivision of hV5/MT+, MST/TO-2 produced the reverse effects, disrupting radial direction discrimination but eliciting no effect on the FOE positional judgment task. This double dissociation demonstrates that FOE position and radial direction of optic flow stimuli are signaled independently by neural activity in areas hV5/MT+ and V3A.NEW & NOTEWORTHY Optic flow constitutes a biologically relevant visual cue as we move through any environment. With the use of neuroimaging and brain-stimulation techniques, this study demonstrates that separate human brain areas are involved in the analysis of the direction of radial motion and the focus of expansion in optic flow. This dissociation reveals the existence of separate processing pathways for the analysis of different attributes of optic flow that are important for the guidance of self-locomotion and object avoidance.

7 tesla FMRI reveals systematic functional organization for binocular disparity in dorsal visual cortex.

The binocular disparity between the views of the world registered by the left and right eyes provides a powerful signal about the depth structure of the environment. Despite increasing knowledge of the cortical areas that process disparity from animal models, comparatively little is known about the local architecture of stereoscopic processing in the human brain. Here, we take advantage of the high spatial specificity and image contrast offered by 7 tesla fMRI to test for systematic organization of disparity representations in the human brain. Participants viewed random dot stereogram stimuli depicting different depth positions while we recorded fMRI responses from dorsomedial visual cortex. We repeated measurements across three separate imaging sessions. Using a series of computational modeling approaches, we report three main advances in understanding disparity organization in the human brain. First, we show that disparity preferences are clustered and that this organization persists across imaging sessions, particularly in area V3A. Second, we observe differences between the local distribution of voxel responses in early and dorsomedial visual areas, suggesting different cortical organization. Third, using modeling of voxel responses, we show that higher dorsal areas (V3A, V3B/KO) have properties that are characteristic of human depth judgments: a simple model that uses tuning parameters estimated from fMRI data captures known variations in human psychophysical performance. Together, these findings indicate that human dorsal visual cortex contains selective cortical structures for disparity that may support the neural computations that underlie depth perception.

The neural representation of objects formed through the spatiotemporal integration of visual transients.

Oftentimes, objects are only partially and transiently visible as parts of them become occluded during observer or object motion. The visual system can integrate such object fragments across space and time into perceptual wholes or spatiotemporal objects. This integrative and dynamic process may involve both ventral and dorsal visual processing pathways, along which shape and spatial representations are thought to arise. We measured fMRI BOLD response to spatiotemporal objects and used multi-voxel pattern analysis (MVPA) to decode shape information across 20 topographic regions of visual cortex. Object identity could be decoded throughout visual cortex, including intermediate (V3A, V3B, hV4, LO1-2,) and dorsal (TO1-2, and IPS0-1) visual areas. Shape-specific information, therefore, may not be limited to early and ventral visual areas, particularly when it is dynamic and must be integrated. Contrary to the classic view that the representation of objects is the purview of the ventral stream, intermediate and dorsal areas may play a distinct and critical role in the construction of object representations across space and time.

Applying Transcranial Magnetic Stimulation (TMS) Over the Dorsal Visual Pathway Induces Schizophrenia-like Disruption of Perceptual Closure.

Perceptual closure ability is postulated to depend upon rapid transmission of magnocellular information to prefrontal cortex via the dorsal stream. In contrast, illusory contour processing requires only local interactions within primary and ventral stream visual regions, such as lateral occipital complex. Schizophrenia is associated with deficits in perceptual closure versus illusory contours processing that is hypothesized to reflect impaired magnocellular/dorsal stream. Perceptual closure and illusory contours performance was evaluated in separate groups of 12 healthy volunteers during no TMS, and during repetitive 10 Hz rTMS stimulation over dorsal stream or vertex (TMS-vertex). Perceptual closure and illusory contours were performed in 11 schizophrenia patients, no TMS was applied in these patients. TMS effects were evaluated with repeated measures ANOVA across treatments. rTMS significantly increased perceptual closure identification thresholds, with significant difference between TMS-dorsal stream and no TMS. TMS-dorsal stream also significantly reduced perceptual closure but not illusory contours accuracy. Schizophrenia patients showed increased perceptual closure identification thresholds relative to controls in the no TMS condition, but similar to controls in the TMS-dorsal stream condition. Conclusions of this study are that magnocellular/dorsal stream input is critical for perceptual closure but not illusory contours performance, supporting both trickledown theories of normal perceptual closure function, and magnocellular/dorsal stream theories of visual dysfunction in schizophrenia.

Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation.

Recent computational models suggest that visual input from optic flow provides information about egocentric (navigator-centered) motion and influences firing patterns in spatially tuned cells during navigation. Computationally, self-motion cues can be extracted from optic flow during navigation. Despite the importance of optic flow to navigation, a functional link between brain regions sensitive to optic flow and brain regions important for navigation has not been established in either humans or animals. Here, we used a beta-series correlation methodology coupled with two fMRI tasks to establish this functional link during goal-directed navigation in humans. Functionally defined optic flow sensitive cortical areas V3A, V6, and hMT+ were used as seed regions. fMRI data was collected during a navigation task in which participants updated position and orientation based on self-motion cues to successfully navigate to an encoded goal location. The results demonstrate that goal-directed navigation requiring updating of position and orientation in the first person perspective involves a cooperative interaction between optic flow sensitive regions V3A, V6, and hMT+ and the hippocampus, retrosplenial cortex, posterior parietal cortex, and medial prefrontal cortex. These functional connections suggest a dynamic interaction between these systems to support goal-directed navigation.

Orienting of visuo-spatial attention in complex 3D space: Search and detection.

The ability to detect changes in the environment is necessary for appropriate interactions with the external world. Changes in the background go more unnoticed than foreground changes, possibly because attention prioritizes processing of foreground/near stimuli. Here, we investigated the detectability of foreground and background changes within natural scenes and the influence of stereoscopic depth cues on this. Using a flicker paradigm, we alternated a pair of images that were exactly same or differed for one single element (i.e., a color change of one object in the scene). The participants were asked to find the change that occurred either in a foreground or background object, while viewing the stimuli either with binocular and monocular cues (bmC) or monocular cues only (mC). The behavioral results showed faster and more accurate detections for foreground changes and overall better performance in bmC than mC conditions. The imaging results highlighted the involvement of fronto-parietal attention controlling networks during active search and target detection. These attention networks did not show any differential effect as function of the presence/absence of the binocular cues, or the detection of foreground/background changes. By contrast, the lateral occipital cortex showed greater activation for detections in foreground compared to background, while area V3A showed a main effect of bmC vs. mC, specifically during search. These findings indicate that visual search with binocular cues does not impose any specific requirement on attention-controlling fronto-parietal networks, while the enhanced detection of front/near objects in the bmC condition reflects bottom-up sensory processes in visual cortex.

Visual field asymmetries in visual evoked responses.

Behavioral responses to visual stimuli exhibit visual field asymmetries, but cortical folding and the close proximity of visual cortical areas make electrophysiological comparisons between different stimulus locations problematic. Retinotopy-constrained source estimation (RCSE) uses distributed dipole models simultaneously constrained by multiple stimulus locations to provide separation between individual visual areas that is not possible with conventional source estimation methods. Magnetoencephalography and RCSE were used to estimate time courses of activity in V1, V2, V3, and V3A. Responses to left and right hemifield stimuli were not significantly different. Peak latencies for peripheral stimuli were significantly shorter than those for perifoveal stimuli in V1, V2, and V3A, likely related to the greater proportion of magnocellular input to V1 in the periphery. Consistent with previous results, sensor magnitudes for lower field stimuli were about twice as large as for upper field, which is only partially explained by the proximity to sensors for lower field cortical sources in V1, V2, and V3. V3A exhibited both latency and amplitude differences for upper and lower field responses. There were no differences for V3, consistent with previous suggestions that dorsal and ventral V3 are two halves of a single visual area, rather than distinct areas V3 and VP.

Neural Selectivity for Visual Motion in Macaque Area V3A.

The processing of visual motion is conducted by dedicated pathways in the primate brain. These pathways originate with populations of direction-selective neurons in the primary visual cortex, which projects to dorsal structures like the middle temporal (MT) and medial superior temporal (MST) areas. Anatomical and imaging studies have suggested that area V3A might also be specialized for motion processing, but there have been very few studies of single-neuron direction selectivity in this area. We have therefore performed electrophysiological recordings from V3A neurons in two macaque monkeys (one male and one female) and measured responses to a large battery of motion stimuli that includes translation motion, as well as more complex optic flow patterns. For comparison, we simultaneously recorded the responses of MT neurons to the same stimuli. Surprisingly, we find that overall levels of direction selectivity are similar in V3A and MT and moreover that the population of V3A neurons exhibits somewhat greater selectivity for optic flow patterns. These results suggest that V3A should be considered as part of the motion processing machinery of the visual cortex, in both human and non-human primates.

A common neural substrate for processing scenes and egomotion-compatible visual motion.

Neuroimaging studies have revealed two separate classes of category-selective regions specialized in optic flow (egomotion-compatible) processing and in scene/place perception. Despite the importance of both optic flow and scene/place recognition to estimate changes in position and orientation within the environment during self-motion, the possible functional link between egomotion- and scene-selective regions has not yet been established. Here we reanalyzed functional magnetic resonance images from a large sample of participants performing two well-known "localizer" fMRI experiments, consisting in passive viewing of navigationally relevant stimuli such as buildings and places (scene/place stimulus) and coherently moving fields of dots simulating the visual stimulation during self-motion (flow fields). After interrogating the egomotion-selective areas with respect to the scene/place stimulus and the scene-selective areas with respect to flow fields, we found that the egomotion-selective areas V6+ and pIPS/V3A responded bilaterally more to scenes/places compared to faces, and all the scene-selective areas (parahippocampal place area or PPA, retrosplenial complex or RSC, and occipital place area or OPA) responded more to egomotion-compatible optic flow compared to random motion. The conjunction analysis between scene/place and flow field stimuli revealed that the most important focus of common activation was found in the dorsolateral parieto-occipital cortex, spanning the scene-selective OPA and the egomotion-selective pIPS/V3A. Individual inspection of the relative locations of these two regions revealed a partial overlap and a similar response profile to an independent low-level visual motion stimulus, suggesting that OPA and pIPS/V3A may be part of a unique motion-selective complex specialized in encoding both egomotion- and scene-relevant information, likely for the control of navigation in a structured environment.

Choice-Related Activity during Visual Slant Discrimination in Macaque CIP But Not V3A.

Creating three-dimensional (3D) representations of the world from two-dimensional retinal images is fundamental to visually guided behaviors including reaching and grasping. A critical component of this process is determining the 3D orientation of objects. Previous studies have shown that neurons in the caudal intraparietal area (CIP) of the macaque monkey represent 3D planar surface orientation (i.e., slant and tilt). Here we compare the responses of neurons in areas V3A (which is implicated in 3D visual processing and precedes CIP in the visual hierarchy) and CIP to 3D-oriented planar surfaces. We then examine whether activity in these areas correlates with perception during a fine slant discrimination task in which the monkeys report if the top of a surface is slanted toward or away from them. Although we find that V3A and CIP neurons show similar sensitivity to planar surface orientation, significant choice-related activity during the slant discrimination task is rare in V3A but prominent in CIP. These results implicate both V3A and CIP in the representation of 3D surface orientation, and suggest a functional dissociation between the areas based on slant-related choice signals.

Neuroanatomical substrates underlying contrast sensitivity.

BACKGROUND: Contrast sensitivity (CS), a measurement of the ability to discriminate an object from its background, is an essential domain of visual functions. Eye aging or diseases are usually responsible for CS decline or impairment. However, whether neuroanatomical substrates are underlying CS is mostly unknown. METHODS: High-resolution magnetic resonance imaging data of 100 healthy young subjects from the Human Connectome Project (HCP) dataset were used to calculate gray matter volume (GMV). CS was assessed using the Mars Contrast Sensitivity Test. A multiple regression analysis was used to investigate the relationship between CS and GMV in a voxel-wise manner within the whole gray matter. RESULTS: The range of Mars_Final scores for the 100 participants was from 1.08 to 1.88, and we found significant positive correlations between the CS scores and GMV in the bilateral visual cortex. Precisely, the significant bilateral clusters were mainly located in bilateral V3A, with the superior parts extending to the bilateral posterior parietal cortex. CONCLUSIONS: These findings suggest the critical role of the dorsal visual stream in CS processing, which may provide insights into the neuroanatomical mechanism of contrast sensitivity and its relation to some brain disorders.

The resonant brain: How attentive conscious seeing regulates action sequences that interact with attentive cognitive learning, recognition, and prediction.

This article describes mechanistic links that exist in advanced brains between processes that regulate conscious attention, seeing, and knowing, and those that regulate looking and reaching. These mechanistic links arise from basic properties of brain design principles such as complementary computing, hierarchical resolution of uncertainty, and adaptive resonance. These principles require conscious states to mark perceptual and cognitive representations that are complete, context sensitive, and stable enough to control effective actions. Surface-shroud resonances support conscious seeing and action, whereas feature-category resonances support learning, recognition, and prediction of invariant object categories. Feedback interactions between cortical areas such as peristriate visual cortical areas V2, V3A, and V4, and the lateral intraparietal area (LIP) and inferior parietal sulcus (IPS) of the posterior parietal cortex (PPC) control sequences of saccadic eye movements that foveate salient features of attended objects and thereby drive invariant object category learning. Learned categories can, in turn, prime the objects and features that are attended and searched. These interactions coordinate processes of spatial and object attention, figure-ground separation, predictive remapping, invariant object category learning, and visual search. They create a foundation for learning to control motor-equivalent arm movement sequences, and for storing these sequences in cognitive working memories that can trigger the learning of cognitive plans with which to read out skilled movement sequences. Cognitive-emotional interactions that are regulated by reinforcement learning can then help to select the plans that control actions most likely to acquire valued goal objects in different situations. Many interdisciplinary psychological and neurobiological data about conscious and unconscious behaviors in normal individuals and clinical patients have been explained in terms of these concepts and mechanisms.

Visual Field Map Clusters in High-Order Visual Processing: Organization of V3A/V3B and a New Cloverleaf Cluster in the Posterior Superior Temporal Sulcus.

The cortical hierarchy of the human visual system has been shown to be organized around retinal spatial coordinates throughout much of low- and mid-level visual processing. These regions contain visual field maps (VFMs) that each follows the organization of the retina, with neighboring aspects of the visual field processed in neighboring cortical locations. On a larger, macrostructural scale, groups of such sensory cortical field maps (CFMs) in both the visual and auditory systems are organized into roughly circular cloverleaf clusters. CFMs within clusters tend to share properties such as receptive field distribution, cortical magnification, and processing specialization. Here we use fMRI and population receptive field (pRF) modeling to investigate the extent of VFM and cluster organization with an examination of higher-level visual processing in temporal cortex and compare these measurements to mid-level visual processing in dorsal occipital cortex. In human temporal cortex, the posterior superior temporal sulcus (pSTS) has been implicated in various neuroimaging studies as subserving higher-order vision, including face processing, biological motion perception, and multimodal audiovisual integration. In human dorsal occipital cortex, the transverse occipital sulcus (TOS) contains the V3A/B cluster, which comprises two VFMs subserving mid-level motion perception and visuospatial attention. For the first time, we present the organization of VFMs in pSTS in a cloverleaf cluster. This pSTS cluster contains four VFMs bilaterally: pSTS-1:4. We characterize these pSTS VFMs as relatively small at ∼125 mm2 with relatively large pRF sizes of ∼2-8° of visual angle across the central 10° of the visual field. V3A and V3B are ∼230 mm2 in surface area, with pRF sizes here similarly ∼1-8° of visual angle across the same region. In addition, cortical magnification measurements show that a larger extent of the pSTS VFM surface areas are devoted to the peripheral visual field than those in the V3A/B cluster. Reliability measurements of VFMs in pSTS and V3A/B reveal that these cloverleaf clusters are remarkably consistent and functionally differentiable. Our findings add to the growing number of measurements of widespread sensory CFMs organized into cloverleaf clusters, indicating that CFMs and cloverleaf clusters may both be fundamental organizing principles in cortical sensory processing.

Cognitive-motor brain-machine interfaces.

Brain-machine interfaces (BMIs) open new horizons for the treatment of paralyzed persons, giving hope for the artificial restoration of lost physiological functions. Whereas BMI development has mainly focused on motor rehabilitation, recent studies have suggested that higher cognitive functions can also be deciphered from brain activity, bypassing low level planning and execution functions, and replacing them by computer-controlled effectors. This review describes the new generation of cognitive-motor BMIs, focusing on three BMI types: By outlining recent progress in developing these BMI types, we aim to provide a unified view of contemporary research towards the replacement of behavioral outputs of cognitive processes by direct interaction with the brain.

Visual perception of axes of head rotation.

Registration of ego-motion is important to accurately navigate through space. Movements of the head and eye relative to space are registered through the vestibular system and optical flow, respectively. Here, we address three questions concerning the visual registration of self-rotation. (1) Eye-in-head movements provide a link between the motion signals received by sensors in the moving eye and sensors in the moving head. How are these signals combined into an ego-rotation percept? We combined optic flow of simulated forward and rotational motion of the eye with different levels of eye-in-head rotation for a stationary head. We dissociated simulated gaze rotation and head rotation by different levels of eye-in-head pursuit. We found that perceived rotation matches simulated head- not gaze-rotation. This rejects a model for perceived self-rotation that relies on the rotation of the gaze line. Rather, eye-in-head signals serve to transform the optic flow's rotation information, that specifies rotation of the scene relative to the eye, into a rotation relative to the head. This suggests that transformed visual self-rotation signals may combine with vestibular signals. (2) Do transformed visual self-rotation signals reflect the arrangement of the semi-circular canals (SCC)? Previously, we found sub-regions within MST and V6(+) that respond to the speed of the simulated head rotation. Here, we re-analyzed those Blood oxygenated level-dependent (BOLD) signals for the presence of a spatial dissociation related to the axes of visually simulated head rotation, such as have been found in sub-cortical regions of various animals. Contrary, we found a rather uniform BOLD response to simulated rotation along the three SCC axes. (3) We investigated if subject's sensitivity to the direction of the head rotation axis shows SCC axes specifcity. We found that sensitivity to head rotation is rather uniformly distributed, suggesting that in human cortex, visuo-vestibular integration is not arranged into the SCC frame.

Nonconscious processing and a novel target for schizophrenia research.

Analysis of the pattern of altered cognition observed in schizophrenia provides better insight into neurocognitive deficits. It reveals a potential novel target for schizophrenia research. To understand this target we reviewed the findings of neuroimaging studies on implicit [nonconscious] memory. These studies have consistently reported attenuated activity in the area V3A of the extrastriate cortex during retrieval of studied items. It was suggested that the attenuation limits the pool of information available for further cognitive processing. Therefore, if V3A is functionally damaged, individuals will have access to a larger pool of information for cognitive processing. Since cognitive tasks that are not dependent on attention [attention independent] process a larger pool of information more efficiently, performance in these tasks is likely to improve after V3A is damaged. Conversely, tasks that are dependent on attentional resources are more efficient in processing smaller pool of information. Performance in these tasks therefore is expected to deteriorate if a large pool of information is made available following V3A damage. A review of cognitive performance in schizophrenia suggests that patients perform at above normal level in attention independent priming tasks and perform at subnormal level in attention dependent episodic and working memory tasks. These findings indicate possible impairment of V3A activity. It could therefore be a potentially important unstudied target for schizophrenia research, particularly because a number of investigators have reported that the activity in this area is altered in schizophrenia.

Does Area V3A Predict Positions of Moving Objects?

A gradually fading moving object is perceived to disappear at positions beyond its luminance detection threshold, whereas abrupt offsets are usually localized accurately. What role does retinotopic activity in visual cortex play in this motion-induced mislocalization of the endpoint of fading objects? Using functional magnetic resonance imaging (fMRI), we localized regions of interest (ROIs) in retinotopic maps abutting the trajectory endpoint of a bar moving either toward or away from this position while gradually decreasing or increasing in luminance. Area V3A showed predictive activity, with stronger fMRI responses for motion toward versus away from the ROI. This effect was independent of the change in luminance. In Area V1 we found higher activity for high-contrast onsets and offsets near the ROI, but no significant differences between motion directions. We suggest that perceived final positions of moving objects are based on an interplay of predictive position representations in higher motion-sensitive retinotopic areas and offset transients in primary visual cortex.

The representation of object distance: evidence from neuroimaging and neuropsychology.

Perceived distance in two-dimensional (2D) images relies on monocular distance cues. Here, we examined the representation of perceived object distance using a continuous carry-over adaptation design for fMRI. The task was to look at photographs of objects and make a judgment as to whether or not the item belonged in the kitchen. Importantly, this task was orthogonal to the variable of interest: the object's perceived distance from the viewer. In Experiment 1, whole brain group analyses identified bilateral clusters in the superior occipital gyrus (approximately area V3/V3A) that showed parametric adaptation to relative changes in perceived distance. In Experiment 2, retinotopic analyses confirmed that area V3A/B reflected the greatest magnitude of response to monocular changes in perceived distance. In Experiment 3, we report that the functional activations overlap with the occipito-parietal lesions in a patient with impaired distance perception, showing that the same regions monitor implied (2D) and actual (three-dimensional) distance. These data suggest that distance information is automatically processed even when it is task-irrelevant and that this process relies on superior occipital areas in and around area V3A.