Integration of Motion Responses Underlying Directional Motion Anisotropy in Human Early Visual Cortical Areas

Recent imaging studies have reported directional motion biases in human visual cortex when perceiving moving random dot patterns. It has been hypothesized that these biases occur as a result of the integration of motion detector activation along the path of motion in visual cortex. In this study we investigate the nature of such motion integration with functional MRI (fMRI) using different motion stimuli. Three types of moving random dot stimuli were presented, showing either coherent motion, motion with spatial decorrelations or motion with temporal decorrelations. The results from the coherent motion stimulus reproduced the centripetal and centrifugal directional motion biases in V1, V2 and V3 as previously reported. The temporally decorrelated motion stimulus resulted in both centripetal and centrifugal biases similar to coherent motion. In contrast, the spatially decorrelated motion stimulus resulted in small directional motion biases that were only present in parts of visual cortex coding for higher eccentricities of the visual field. In combination with previous results, these findings indicate that biased motion responses in early visual cortical areas most likely depend on the spatial integration of a simultaneously activated motion detector chain.     

The neural basis of centre-surround interactions in visual motion processing

Perception of a moving visual stimulus can be suppressed or enhanced by surrounding context in adjacent parts of the visual field. We studied the neural processes underlying such contextual modulation with fMRI. We selected motion selective regions of interest (ROI) in the occipital and parietal lobes with sufficiently well defined topography to preclude direct activation by the surround. BOLD signal in the ROIs was suppressed when surround motion direction matched central stimulus direction, and increased when it was opposite. With the exception of hMT+/V5, inserting a gap between the stimulus and the surround abolished surround modulation. This dissociation between hMT+/V5 and other motion selective regions prompted us to ask whether motion perception is closely linked to processing in hMT+/V5, or reflects the net activity across all motion selective cortex. The motion aftereffect (MAE) provided a measure of motion perception, and the same stimulus configurations that were used in the fMRI experiments served as adapters. Using a linear model, we found that the MAE was predicted more accurately by the BOLD signal in hMT+/V5 than it was by the BOLD signal in other motion selective regions. However, a substantial improvement in prediction accuracy could be achieved by using the net activity across all motion selective cortex as a predictor, suggesting the overall conclusion that visual motion perception depends upon the integration of activity across different areas of visual cortex.     

Human V6: Functional Characterisation and Localisation

Human visual area V6, in the parieto-occipital sulcus, is thought to have an important role in the extraction of optic flow for the monitoring and guidance of self-motion (egomotion) because it responds differentially to egomotion-compatible optic flow when compared to: (a) coherent but egomotion-incompatible flow (Cardin & Smith, 2010), and (b) incoherent motion (Pitzalis et al., 2010). It is not clear, however, whether V6 responds more strongly to egomotion-incompatible global motion than to incoherent motion. This is relevant not only for determining the functional properties of V6, but also in order to choose optimal stimuli for localising V6 accurately with fMRI. Localisation with retinotopic mapping is difficult and there is a need for a simple, reliable method. We conducted an event-related 3T fMRI experiment in which participants viewed a display of dots which either: a) followed a time-varying optic flow trajectory in a single, egomotion-compatible (EC) display; b) formed an egomotion-incompatible (EI) 3×3 array of optic flow patches; or c) moved randomly (RM). Results from V6 show an ordering of response magnitudes: EC > EI > RM. Neighbouring areas V3A and V7 responded more strongly to EC than to RM, but about equally to EC and EI. Our results suggest that although V6 may have a general role in the extraction of global motion, in clear contrast to neighbouring motion areas it is especially concerned with encoding EC stimuli. They suggest two strategies for localising V6: (1) contrasting EC and EI; or (2) contrasting EC and RM, which is more sensitive but carries a risk of including voxels from neighbouring regions that also show a EC > RM preference.     

Direction repulsion goes global

When viewing two superimposed, translating sets of dots moving in different directions, one overestimates direction difference. This phenomenon of direction repulsion is thought to be driven by inhibitory interactions between directionally tuned motion detectors. However, there is disagreement on where this occurs-at early stages of motion processing, when local motions are extracted; or at the later, global motion-processing stage following "pooling" of these local measures. These two stages of motion processing have been identified as occurring in area V1 and the human homolog of macaque MT/V5, respectively. We designed experiments in which local and global predictions of repulsion are pitted against one another. Our stimuli contained a target set of dots, moving at a uniform speed, superimposed on a "mixed-speed" distractor set. Because the perceived speed of a mixed-speed stimulus is equal to the dots' average speed, a global-processing account of direction repulsion predicts that repulsion magnitude induced by a mixed-speed distractor will be indistinguishable from that induced by a single-speed distractor moving at the same mean speed. This is exactly what we found. These results provide compelling evidence that global-motion interactions play a major role in driving direction repulsion.     

Human cortical regions involved in extracting depth from motion

We used functional magnetic resonance imaging (fMRI) to investigate brain regions involved in extracting three-dimensional structure from motion. A factorial design included two-dimensional and three-dimensional structures undergoing rigid and nonrigid motions. As predicted from monkey data, the human homolog of MT/V5 was significantly more active when subjects viewed three-dimensional (as opposed to two-dimensional) displays, irrespective of their rigidity. Human MT/V5+ (hMT/V5+) is part of a network with right hemisphere dominance involved in extracting depth from motion, including a lateral occipital region, five sites along the intraparietal sulcus (IPS), and two ventral occipital regions. Control experiments confirmed that this pattern of activation is most strongly correlated with perceived three-dimensional structure, in as much as it arises from motion and cannot be attributed to numerous two-dimensional image properties or to saliency.     

Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain

There is much evidence in primates' visual processing for distinct mechanisms involved in object recognition and encoding object position and motion, which have been identified with 'ventral' and 'dorsal' streams, respectively, of the extra-striate visual areas [1] [2] [3]. This distinction may yield insights into normal human perception, its development and pathology. Motion coherence sensitivity has been taken as a test of global processing in the dorsal stream [4] [5]. We have proposed an analogous 'form coherence' measure of global processing in the ventral stream [6]. In a functional magnetic resonance imaging (fMRI) experiment, we found that the cortical regions activated by form coherence did not overlap with those activated by motion coherence in the same individuals. Areas differentially activated by form coherence included regions in the middle occipital gyrus, the ventral occipital surface, the intraparietal sulcus, and the temporal lobe. Motion coherence activated areas consistent with those previously identified as V5 and V3a, the ventral occipital surface, the intraparietal sulcus, and temporal structures. Neither form nor motion coherence activated area V1 differentially. Form and motion foci in occipital, parietal, and temporal areas were nearby but showed almost no overlap. These results support the idea that form and motion coherence test distinct functional brain systems, but that these do not necessarily correspond to a gross anatomical separation of dorsal and ventral processing streams.     

Tactile motion and pattern processing assessed with high-field FMRI

Processing of motion and pattern has been extensively studied in the visual domain, but much less in the somatosensory system. Here, we used ultra-high-field functional magnetic resonance imaging (fMRI) at 7 Tesla to investigate the neuronal correlates of tactile motion and pattern processing in humans under tightly controlled stimulation conditions. Different types of dynamic stimuli created the sensation of moving or stationary bar patterns during passive touch. Activity in somatosensory cortex was increased during both motion and pattern processing and modulated by motion directionality in primary and secondary somatosensory cortices (SI and SII) as well as by pattern orientation in the anterior intraparietal sulcus. Furthermore, tactile motion and pattern processing induced activity in the middle temporal cortex (hMT+/V5) and in the inferior parietal cortex (IPC), involving parts of the supramarginal und angular gyri. These responses covaried with subjects' individual perceptual performance, suggesting that hMT+/V5 and IPC contribute to conscious perception of specific tactile stimulus features. In addition, an analysis of effective connectivity using psychophysiological interactions (PPI) revealed increased functional coupling between SI and hMT+/V5 during motion processing, as well as between SI and IPC during pattern processing. This connectivity pattern provides evidence for the direct engagement of these specialized cortical areas in tactile processing during somesthesis.     

Seeing invisible motion: a human FMRI study

A common view about visual consciousness is that it could arise when and where activity reaches some higher level of processing along the cortical hierarchy. Reports showing that activity in striate cortex can be dissociated from awareness , whereas the latter modulates activity in higher areas , point in this direction. In the specific case of visual motion, a central, "perceptual" role has been assigned to area V5: several human and monkey studies have shown V5 activity to correlate with the motion percept. Here we show that activity in this and other higher cortical areas can be also dissociated from perception and follow the physical stimulus instead. The motion information in a peripheral grating modulated fMRI responses, despite being invisible to human volunteers: under crowding conditions , areas V3A, V5, and parietal cortex still showed increased activity when the grating was moving compared to when it was flickering. We conclude that stimulus-specific activation of higher cortical areas does not necessarily result in awareness of the underlying stimulus.     

Activation of Multimodal Areas in the Human Cerebral Cortex in Response to Biological Motion Sounds

Functional magnetic resonance imaging (fMRI) was used to investigate activation of the multimodal areas in the cerebral cortex–supramarginal and angular gyri, precuneus, and middle temporal visual cortex (MT/V5)–in response to motion of biologically significant sounds (human footsteps). The subjects listened to approaching or receding footstep sounds during 45 s, and such stimulation was supposed to evoke auditory adaptation to biological motion. Listening conditions alternated with stimulation-free control. To reveal activity in the regions of interest, the periods before and during stimulation were compared. Most stable and voluminous activation was detected in the supramarginal and angular gyri, being registered for all footstep sound types–approaching, receding and steps in place. Listening to human approaching steps activated the precuneus area, with the volume of activation clusters varying considerably between subjects. In the MT/V5 area, activation was revealed in 5 of 21 subjects. The involvement of the tested multimodal cortical areas in analyzing biological motion is discussed.     

Selectivity to Translational Egomotion in Human Brain Motion Areas

The optic flow generated when a person moves through the environment can be locally decomposed into several basic components, including radial, circular, translational and spiral motion. Since their analysis plays an important part in the visual perception and control of locomotion and posture it is likely that some brain regions in the primate dorsal visual pathway are specialized to distinguish among them. The aim of this study is to explore the sensitivity to different types of egomotion-compatible visual stimulations in the human motion-sensitive regions of the brain. Event-related fMRI experiments, 3D motion and wide-field stimulation, functional localizers and brain mapping methods were used to study the sensitivity of six distinct motion areas (V6, MT, MST+, V3A, CSv and an Intra-Parietal Sulcus motion [IPSmot] region) to different types of optic flow stimuli. Results show that only areas V6, MST+ and IPSmot are specialized in distinguishing among the various types of flow patterns, with a high response for the translational flow which was maximum in V6 and IPSmot and less marked in MST+. Given that during egomotion the translational optic flow conveys differential information about the near and far external objects, areas V6 and IPSmot likely process visual egomotion signals to extract information about the relative distance of objects with respect to the observer. Since area V6 is also involved in distinguishing object-motion from self-motion, it could provide information about location in space of moving and static objects during self-motion, particularly in a dynamically unstable environment.     

Illusions of Visual Motion Elicited by Electrical Stimulation of Human MT Complex

Human cortical area MT⁺ (hMT⁺) is known to respond to visual motion stimuli, but its causal role in the conscious experience of motion remains largely unexplored. Studies in non-human primates demonstrate that altering activity in area MT can influence motion perception judgments, but animal studies are inherently limited in assessing subjective conscious experience. In the current study, we use functional magnetic resonance imaging (fMRI), intracranial electrocorticography (ECoG), and electrical brain stimulation (EBS) in three patients implanted with intracranial electrodes to address the role of area hMT⁺ in conscious visual motion perception. We show that in conscious human subjects, reproducible illusory motion can be elicited by electrical stimulation of hMT⁺. These visual motion percepts only occurred when the site of stimulation overlapped directly with the region of the brain that had increased fMRI and electrophysiological activity during moving compared to static visual stimuli in the same individual subjects. Electrical stimulation in neighboring regions failed to produce illusory motion. Our study provides evidence for the sufficient causal link between the hMT⁺ network and the human conscious experience of visual motion. It also suggests a clear spatial relationship between fMRI signal and ECoG activity in the human brain.     

Separate processing of different global-motion structures in visual cortex is revealed by FMRI

The visual system has the remarkable ability to extract several types of meaningful global-motion signals, such as radial motion, translation motion, and rotation, for different visual functions and actions. In the monkey brain, different groups of cells in MST respond best to different types of global motion [1, 2] whereas in lower cortical areas including MT, no such differential responses have been found. Here, we show that an area (or areas) lower than MST in the human brain [3] responds to different types of global motion. A series of human functional magnetic resonance imaging (fMRI) experiments, in which attention was controlled for, indicated that the center of radial motion activates the corresponding location in the V3A representation, whereas translation motion activates mainly in a more peripheral representation of V3A. These results suggest that in the human brain, V3A is an area that differentially responds according to the type of global motion.     

Decoding seen and attended motion directions from activity in the human visual cortex

Functional neuroimaging has successfully identified brain areas that show greater responses to visual motion and adapted responses to repeated motion directions. However, such methods have been thought to lack the sensitivity and spatial resolution to isolate direction-selective responses to individual motion stimuli. Here, we used functional magnetic resonance imaging (fMRI) and pattern classification methods to show that ensemble activity patterns in human visual cortex contain robust direction-selective information, from which it is possible to decode seen and attended motion directions. Ensemble activity in areas V1-V4 and MT+/V5 allowed us to decode which of eight possible motion directions the subject was viewing on individual stimulus blocks. Moreover, ensemble activity evoked by single motion directions could effectively predict which of two overlapping motion directions was the focus of the subject's attention and presumably dominant in perception. Our results indicate that feature-based attention can bias direction-selective population activity in multiple visual areas, including MT+/V5 and early visual areas (V1-V4), consistent with gain-modulation models of feature-based attention and theories of early attentional selection. Our approach for measuring ensemble direction selectivity may provide new opportunities to investigate relationships between attentional selection, conscious perception, and direction-selective responses in the human brain.     

Spatiotopic coding of BOLD signal in human visual cortex depends on spatial attention

The neural substrate of the phenomenological experience of a stable visual world remains obscure. One possible mechanism would be to construct spatiotopic neural maps where the response is selective to the position of the stimulus in external space, rather than to retinal eccentricities, but evidence for these maps has been inconsistent. Here we show, with fMRI, that when human subjects perform concomitantly a demanding attentive task on stimuli displayed at the fovea, BOLD responses evoked by moving stimuli irrelevant to the task were mostly tuned in retinotopic coordinates. However, under more unconstrained conditions, where subjects could attend easily to the motion stimuli, BOLD responses were tuned not in retinal but in external coordinates (spatiotopic selectivity) in many visual areas, including MT, MST, LO and V6, agreeing with our previous fMRI study. These results indicate that spatial attention may play an important role in mediating spatiotopic selectivity.     

Altered velocity processing in schizophrenia during pursuit eye tracking

Smooth pursuit eye movements (SPEM) are needed to keep the retinal image of slowly moving objects within the fovea. Depending on the task, about 50%-80% of patients with schizophrenia have difficulties in maintaining SPEM. We designed a study that comprised different target velocities as well as testing for internal (extraretinal) guidance of SPEM in the absence of a visual target. We applied event-related fMRI by presenting four velocities (5, 10, 15, 20°/s) both with and without intervals of target blanking. 17 patients and 16 healthy participants were included. Eye movements were registered during scanning sessions. Statistical analysis included mixed ANOVAs and regression analyses of the target velocity on the Blood Oxygen Level Dependency (BOLD) signal. The main effect group and the interaction of velocity×group revealed reduced activation in V5 and putamen but increased activation of cerebellar regions in patients. Regression analysis showed that activation in supplementary eye field, putamen, and cerebellum was not correlated to target velocity in patients in contrast to controls. Furthermore, activation in V5 and in intraparietal sulcus (putative LIP) bilaterally was less strongly correlated to target velocity in patients than controls. Altered correlation of target velocity and neural activation in the cortical network supporting SPEM (V5, SEF, LIP, putamen) implies impaired transformation of the visual motion signal into an adequate motor command in patients. Cerebellar regions seem to be involved in compensatory mechanisms although cerebellar activity in patients was not related to target velocity.     

Low-level visual processing of biological motion.

Biological motion displays depict a moving human figure by means of just a few isolated points of light attached to the major joints of the body. Naive observers readily interpret the moving pattern of dots as representing a human figure, despite the complete absence of form cues. This paper reports a series of experiments which investigated the visual processes underlying the phenomenon. Results suggest that (i) the effect relies upon responses in low-level motion-detecting processes, which operate over short temporal and spatial intervals and respond to local modulations in image intensity; and (ii) the effect does not involve hierarchical visual analysis of motion components, nor does it require the presence of dots which move in rigid relation to each other. Instead, movements of the extremities are crucial. Data are inconsistent with current theoretical treatments.     

The Extraction of Depth Structure from Shading and Texture in the Macaque Brain

We used contrast-agent enhanced functional magnetic resonance imaging (fMRI) in the alert monkey to map the cortical regions involved in the extraction of 3D shape from the monocular static cues, texture and shading. As in the parallel human imaging study [1], we contrasted the 3D condition to several 2D control conditions. The extraction of 3D shape from texture (3D SfT) involves both ventral and parietal regions, in addition to early visual areas. Strongest activation was observed in CIP, with decreasing strength towards the anterior part of the intraparietal sulcus (IPS). In the ventral stream 3D SfT sensitivity was observed in a ventral portion of TEO. The extraction of 3D shape from shading (3D SfS) involved predominantly ventral regions, such as V4 and a dorsal potion of TEO. These results are similar to those obtained earlier in human subjects and indicate that the extraction of 3D shape from texture is performed in both ventral and dorsal regions for both species, as are the motion and disparity cues, whereas shading is mainly processed in the ventral stream.     

Individual differences among grapheme-color synesthetes: brain-behavior correlations

Grapheme-color synesthetes experience specific colors associated with specific number or letter characters. To determine the neural locus of this condition, we compared behavioral and fMRI responses in six grapheme-color synesthetes to control subjects. In our behavioral experiments, we found that a subject's synesthetic experience can aid in texture segregation (experiment 1) and reduce the effects of crowding (experiment 2). For synesthetes, graphemes produced larger fMRI responses in color-selective area human V4 than for control subjects (experiment 3). Importantly, we found a correlation within subjects between the behavioral and fMRI results; subjects with better performance on the behavioral experiments showed larger fMRI responses in early retinotopic visual areas (V1, V2, V3, and hV4). These results suggest that grapheme-color synesthesia is the result of cross-activation between grapheme-selective and color-selective brain areas. The correlation between the behavioral and fMRI results suggests that grapheme-color synesthetes may constitute a heterogeneous group.     

Performance Characterization of Watson Ahumada Motion Detector Using Random Dot Rotary Motion Stimuli

The performance of Watson & Ahumada''s model of human visual motion sensing is compared against human psychophysical performance. The stimulus consists of random dots undergoing rotary motion, displayed in a circular annulus. The model matches psychophysical observer performance with respect to most parameters. It is able to replicate some key psychophysical findings such as invariance of observer performance to dot density in the display, and decrease of observer performance with frame duration of the display.Associated with the concept of rotary motion is the notion of a center about which rotation occurs. One might think that for accurate estimation of rotary motion in the display, this center must be accurately known. A simple vector analysis reveals that this need not be the case. Numerical simulations confirm this result, and may explain the position invariance of MST(d) cells. Position invariance is the experimental finding that rotary motion sensitive cells are insensitive to where in their receptive field rotation occurs.When all the dots in the display are randomly drawn from a uniform distribution, illusory rotary motion is perceived. This case was investigated by Rose & Blake previously, who termed the illusory rotary motion the omega effect. Two important experimental findings are reported concerning this effect. First, although the display of random dots evokes perception of rotary motion, the direction of motion perceived does not depend on what dot pattern is shown. Second, the time interval between spontaneous flips in perceived direction is lognormally distributed (mode≈2 s). These findings suggest the omega effect fits in the category of a typical bistable illusion, and therefore the processes that give rise to this illusion may be the same processes that underlie much of other bistable phenomenon.     

Intrapatient alterations in the human immunodeficiency virus type 1 gp120 V1V2 and V3 regions differentially modulate coreceptor usage, virus inhibition by CC/CXC chemokines, soluble CD4, and the b12 and 2G12 monoclonal antibodies

We studied human immunodeficiency virus type 1 (HIV-1) chimeric viruses altering in their gp120 V1V2 and V3 envelope regions to better map which genetic alterations are associated with specific virus phenotypes associated with HIV-1 disease progression. The V1V2 and V3 regions studied were based on viruses isolated from an individual with progressing HIV-1 disease. Higher V3 charges were linked with CXCR4 usage, but only when considered within a specific V1V2 and V3 N-linked glycosylation context. When the virus gained R5X4 dual tropism, irrespective of its V3 charge, it became highly resistant to inhibition by RANTES and highly sensitive to inhibition by SDF-1alpha. R5 viruses with higher positive V3 charges were more sensitive to inhibition by RANTES, while R5X4 dualtropic viruses with higher positive V3 charges were more resistant to inhibition by SDF-1alpha. Loss of the V3 N-linked glycosylation event rendered the virus more resistant to inhibition by SDF-1alpha. The same alterations in the V1V2 and V3 regions influenced the extent to which the viruses were neutralized with soluble CD4, as well as monoclonal antibodies b12 and 2G12, but not monoclonal antibody 2F5. These results further identify a complex set of alterations within the V1V2 and V3 regions of HIV-1 that can be selected in the host via alterations of coreceptor usage, CC/CXC chemokine inhibition, CD4 binding, and antibody neutralization.