Distinct dorsal and ventral streams for binocular rivalry dominance and suppression revealed by magnetoencephalography.

Binocular rivalry is an example of bistable visual perception extensively examined in neuroimaging. Magnetoencephalography can track brain responses to phasic visual stimulations of predetermined frequency and phase to advance our understanding of perceptual dominance and suppression in binocular rivalry. We used left and right eye stimuli that flickered at two tagging frequencies to track their respective oscillatory cortical evoked responses. We computed time-resolved measures of coherence to track brain responses phase locked with stimulus frequencies and with respect to the participants' indications of alternations of visual rivalry they experienced. We compared the brain maps obtained to those from a non-rivalrous control replay condition that used physically changing stimuli to mimic rivalry. We found stronger coherence within a posterior cortical network of visual areas during rivalry dominance compared with rivalry suppression and replay control. This network extended beyond the primary visual cortex to several retinotopic visual areas. Moreover, network coherence with dominant percepts in primary visual cortex peaked at least 50 ms prior to the suppressed percept nadir, consistent with the escape theory of alternations. Individual alternation rates were correlated with the rate of change in dominant evoked peaks, but not for the slope of response to suppressed percepts. Effective connectivity measures revealed that dominant (respectively, suppressed) percepts were expressed in dorsal (respectively ventral) streams. We thus demonstrate that binocular rivalry dominance and suppression engage distinct mechanisms and brain networks. These findings advance neural models of rivalry and may relate to more general aspects of selection and suppression in natural vision.

Interocular Grouping in Perceptual Rivalry Localized with fMRI.

Bistable perception refers to a broad class of dynamically alternating visual illusions that result from ambiguous images. These illusions provide a powerful method to study the mechanisms that determine how visual input is integrated over space and time. Binocular rivalry occurs when subjects view different images in each eye, and a similar experience called stimulus rivalry occurs even when the left and right images are exchanged at a fast rate. Many previous studies have identified with fMRI a network of cortical regions that are recruited during binocular rivalry, relative to non-rivalrous control conditions (termed replay) that use physically changing stimuli to mimic rivalry. However, we show here for the first time that additional cortical areas are activated when subjects experience rivalry with interocular grouping. When interocular grouping occurs, activation levels broadly increase, with a slight shift towards right hemisphere lateralization. Moreover, direct comparison of binocular rivalry with and without grouping highlights strong focused activity in the intraparietal sulcus and lateral occipital areas, such as right-sided retinotopic visual areas LO1 and IP2, as well as activity in left-sided visual areas LO1, and IP0-IP2. The equivalent analyses for comparable stimulus (eye-swap) rivalry showed very similar results; the main difference is greater recruitment of the right superior parietal cortex for binocular rivalry, as previously reported. Thus, we found minimal interaction between the novel networks isolated here for interocular grouping, and those previously attributed to stimulus and binocular rivalry. We conclude that spatial integration (i.e,. image grouping/segmentation) is a key function of lateral occipital/intraparietal cortex that acts similarly on competing binocular stimulus representations, regardless of fast monocular changes.

Tagged MEG measures binocular rivalry in a cortical network that predicts alternation rate.

Binocular rivalry (BR) is a dynamic visual illusion that provides insight into the cortical mechanisms of visual awareness, stimulus selection, and object identification. When dissimilar binocular images cannot be fused, perception switches every few seconds between the left and right eye images. The speed at which individuals switch between alternatives is a stable, partially heritable trait. In order to isolate the monocular and binocular processes that determine the speed of rivalry, we presented stimuli tagged with a different flicker frequency in each eye and applied stimulus-phase locked MEG source imaging. We hypothesized that the strength of the evoked fundamental or intermodulation frequencies would vary when comparing Fast and Slow Switchers. Ten subjects reported perceptual alternations, with mean dominance durations between 1.2-4.0 sec. During BR, event-related monocular input in V1, and broadly in higher-tier ventral temporal cortex, waxed and waned with the periods of left or right eye dominance/suppression. In addition, we show that Slow Switchers produce greater evoked intermodulation frequency responses in a cortical network composed of V1, lateral occipital, posterior STS, retrosplenial & superior parietal cortices. Importantly, these dominance durations were not predictable from the brain responses to either of the fundamental tagging frequencies in isolation, nor from any responses to a pattern rivalry control condition, or a non-rivalrous control. The novel cortical network isolated, which overlaps with the default-mode network, may contain neurons that compute the level of endogenous monocular difference, and monitor accumulation of this conflict over extended periods of time. These findings are the first to relate the speed of rivalry across observers to the 'efficient coding' theory of computing binocular differences that may apply to binocular vision generally.

Transcranial magnetic stimulation to visual cortex induces suboptimal introspection.

Blindsight patients with damage to the visual cortex can discriminate objects but report no conscious visual experience. This provides an intriguing opportunity to allow the study of subjective awareness in isolation from objective performance capacity. However, blindsight is rare, so one promising way to induce the effect in neurologically intact observers is to apply transcranial magnetic stimulation (TMS) to the visual cortex. Here, we used a recently-developed criterion-free method to conclusively rule out an important alternative interpretation of TMS-induced performance without awareness: that TMS-induced blindsight may be just due to conservative reporting biases for conscious perception. Critically, using this criterion-free paradigm we have previously shown that introspective judgments were optimal even under visual masking. However, here under TMS, observers were suboptimal, as if they were metacognitively blind to the visual disturbances caused by TMS. We argue that metacognitive judgments depend on observers' internal statistical models of their own perceptual systems, and introspective suboptimality arises when external perturbations abruptly make those models invalid - a phenomenon that may also be happening in actual blindsight.

Children's Brain Responses to Optic Flow Vary by Pattern Type and Motion Speed.

Structured patterns of global visual motion called optic flow provide crucial information about an observer's speed and direction of self-motion and about the geometry of the environment. Brain and behavioral responses to optic flow undergo considerable postnatal maturation, but relatively little brain imaging evidence describes the time course of development in motion processing systems in early to middle childhood, a time when psychophysical data suggest that there are changes in sensitivity. To fill this gap, electroencephalographic (EEG) responses were recorded in 4- to 8-year-old children who viewed three time-varying optic flow patterns (translation, rotation, and radial expansion/contraction) at three different speeds (2, 4, and 8 deg/s). Modulations of global motion coherence evoked coherent EEG responses at the first harmonic that differed by flow pattern and responses at the third harmonic and dot update rate that varied by speed. Pattern-related responses clustered over right lateral channels while speed-related responses clustered over midline channels. Both children and adults show widespread responses to modulations of motion coherence at the second harmonic that are not selective for pattern or speed. The results suggest that the developing brain segregates the processing of optic flow pattern from speed and that an adult-like pattern of neural responses to optic flow has begun to emerge by early to middle childhood.

Comparison of stimulus rivalry to binocular rivalry with functional magnetic resonance imaging.

When incompatible images are presented to each eye, a phenomenon known as binocular rivalry occurs in which the viewer's conscious visual perception alternates between the two images. In stimulus rivalry, similar perceptual alternations between rival images can occur even in the midst of fast image swapping between the eyes. Here, we used functional magnetic resonance imaging to directly compare brain activity underlying the two types of perceptual rivalry. Overall, we found that activity for binocular rivalry was always stronger and more widespread than that for stimulus rivalry-even more so during passive viewing conditions. In particular, the right superior parietal cortex and the right temporoparietal junction were prominently engaged for passive binocular rivalry. While both types of rivalry engaged higher tier visual regions such as the ventral temporal cortex during an active task, activity for stimulus rivalry was comparatively weak in early visual areas V1 to V3, presumably due to a weaker feed-forward signal due to both intraocular and interocular inhibition that may reduce effective contrast. In sum, only binocular rivalry produced perceptually vivid alternations, increased activation of the early visual cortex, and the coordinated engagement of dorsal stream regions, even when a task was not performed. These findings help characterize how stimulus rivalry fits within hierarchical models of binocular rivalry.

Individual peak gamma frequency predicts switch rate in perceptual rivalry.

Perceptual rivalry-the experience of alternation between two mutually exclusive interpretations of an ambiguous image-provides powerful opportunities to study conscious awareness. It is known that individual subjects experience perceptual alternations for various types of bistable stimuli at distinct rates, and this a stable, heritable trait. Also stable and heritable is the peak frequency of induced gamma-band (30-100 Hz) oscillation of a population-level response in occipital cortex to simple visual patterns, which has been established as a neural correlate of conscious processing. Interestingly, models for rivalry alternation rate and for the frequency of population-level oscillation have both cited inhibitory connections in cortex as crucial determinants of individual differences, and yet the relationship between these two variables has not yet been investigated. Here, we used magnetoencephalography to compare differences in alternation rate for binocular and monocular types of perceptual rivalry to differences in evoked and induced gamma-band frequency of neuromagnetic brain responses to simple nonrivalrous grating stimuli. For both types of bistable images, alternation rate was inversely correlated with the peak frequency of late evoked gamma activity in primary visual cortex (200-400 ms latency). Our results advance models of inhibition that account for subtle variation in normal visual cortex, and shed light on how small differences in anatomy and physiology relate to individual cognition and performance.

Cortical responses to optic flow and motion contrast across patterns and speeds.

Motion provides animals with fast and robust cues for navigation and object detection. In the first case, stereotyped patterns of optic flow inform a moving observer about the direction and speed of its own movement. In the case of object detection, regional differences in motion allow for the segmentation of figures from their background, even in the absence of color or shading cues. Previous research has investigated human electrophysiological responses to global motion across speeds, but only focused upon one type of optic flow pattern. Here, we compared steady-state visual evoked potential (SSVEP) responses across patterns and speeds, both for optic flow and for motion-defined figure patterns, to assess the extent to which the processes are pattern-general or pattern-specific. For optic flow, pattern and speed effects on response amplitudes varied substantially across channels, suggesting pattern-specific processing at slow speeds and pattern-general activity at fast speeds. Responses for coherence- and direction-defined figures were comparatively more uniform, with similar response profiles and spatial distributions. Self- and object-motion patterns activate some of the same circuits, but these data suggest differential sensitivity: not only across the two classes of motion, but also across the patterns within each class, and across speeds. Thus, the results demonstrate that cortical processing of global motion is complex and activates a distributed network.

Long range grouping mechanisms for object perception.

The case made by Kogo and Wagemans for border ownership of surface boundaries to explain modal completion of illusory contours is well argued, and is compatible with psychophysical and physiological research on configural interactions with stereoscopic depth processing. However, it is important to contextualize such a mechanism of surface interpolation with related object grouping mechanisms in visual cortex, such as those not necessarily related to depth. Additionally, it's worth considering how the BOWN model can be generalized beyond Kanizsa shapes to more complex volumetric surface interpolations.

Linking brain to behavior for the visual perception of figures and objects.

The dissociation of a figure from its background is an essential feat of visual perception, as it allows us to detect, recognize, and interact with shapes and objects in our environment. In order to understand how the human brain gives rise to the perception of figures, we here review experiments that explore the links between activity in visual cortex and performance of perceptual tasks related to figure perception. We organize our review according to a proposed model that attempts to contextualize figure processing within the more general framework of object processing in the brain. Overall, the current literature provides us with individual linking hypotheses as to cortical regions that are necessary for particular tasks related to figure perception. Attempts to reach a more complete understanding of how the brain instantiates figure and object perception, however, will have to consider the temporal interaction between the many regions involved, the details of which may vary widely across different tasks.

Defective motion processing in children with cerebral visual impairment due to periventricular white matter damage.

AIM: We sought to characterize visual motion processing in children with cerebral visual impairment (CVI) due to periventricular white matter damage caused by either hydrocephalus (eight individuals) or periventricular leukomalacia (PVL) associated with prematurity (11 individuals). METHOD: Using steady-state visually evoked potentials (ssVEP), we measured cortical activity related to motion processing for two distinct types of visual stimuli: 'local' motion patterns thought to activate mainly primary visual cortex (V1), and 'global' or coherent patterns thought to activate higher cortical visual association areas (V3, V5, etc.). We studied three groups of children: (1) 19 children with CVI (mean age 9y 6mo [SD 3y 8mo]; 9 male; 10 female); (2) 40 neurologically and visually normal comparison children (mean age 9y 6mo [SD 3y 1mo]; 18 male; 22 female); and (3) because strabismus and amblyopia are common in children with CVI, a group of 41 children without neurological problems who had visual deficits due to amblyopia and/or strabismus (mean age 7y 8mo [SD 2y 8mo]; 28 male; 13 female). RESULTS: We found that the processing of global as opposed to local motion was preferentially impaired in individuals with CVI, especially for slower target velocities (p=0.028). INTERPRETATION: Motion processing is impaired in children with CVI. ssVEP may provide useful and objective information about the development of higher visual function in children at risk for CVI.

Distinct cortical responses to 2D figures defined by motion contrast.

Motion contrast contributes to the segregation of a two-dimensional figure from its background, yet many questions remain about its neural mechanisms. We measured steady-state visual evoked potential (SSVEP) responses to moving dot displays in which figure regions emerged from and disappeared into the background at a specific temporal frequency (1.2Hz, F1), based on regional differences of dot direction and global direction coherence. The goal was to measure the cortical response function across a range of motion contrast magnitudes. In two experiments using both a low channel count electrode array (Experiment 1) and a high density array (Experiment 2), we observed two distinct phase-locked evoked responses that were similar across motion contrast type. A response at 1.2Hz (1F1) increased in amplitude with increasing magnitudes of direction or coherence contrast. A response at 2.4Hz (2F1) increased in amplitude, but saturated at low levels of direction or coherence contrast. The two components showed different scalp distributions - the 1F1 was strongest along medial occipital channels, while the 2F1 was bilaterally distributed. Taken together, the studies suggest that figures defined by different types of motion contrast are processed by cortical systems with similar dynamics, and that there are separable neural systems devoted to (i) signaling the absolute magnitude of motion contrast and (ii) detecting when a figure defined by motion contrast appears and disappears from view.