Hiroshi Ban

The integration of motion and disparity cues to depth in dorsal visual cortex

Humans exploit a range of visual depth cues to estimate three-dimensional structure. For example, the slant of a nearby tabletop can be judged by combining information from binocular disparity, texture and perspective. Behavioral tests show humans combine cues near-optimally, a feat that could depend on discriminating the outputs from cue-specific mechanisms or on fusing signals into a common representation. Although fusion is computationally attractive, it poses a substantial challenge, requiring the integration of quantitatively different signals. We used functional magnetic resonance imaging (fMRI) to provide evidence that dorsal visual area V3B/KO meets this challenge. Specifically, we found that fMRI responses are more discriminable when two cues (binocular disparity and relative motion) concurrently signal depth, and that information provided by one cue is diagnostic of depth indicated by the other. This suggests a cortical node important when perceiving depth, and highlights computations based on fusion in the dorsal stream.

Toward a Common Circle: Interhemispheric Contextual Modulation in Human Early Visual Areas

Humans can readily and effortlessly perceive a rich, stable, and unified visual world from a complex visual scene. Yet our internal representation of a visual object appears to be sparse and fragmented. How and where in the brain are such fragmented representations organized into a whole percept? Recent studies have accumulated evidence that some global feature integration is mediated at the early stage of visual processing. However, the spatial operating range of the integration still remains unclear. The present human functional magnetic resonance imaging study provides support that the global integration process in early visual areas, including even the primary visual area V1, is mediated beyond the separated projection of visual hemifields from right and left sides of the fixation to the visual cortex of the contralateral cerebral hemisphere. Retinotopic neural responses corresponding to a visual target were significantly enhanced when another target was simultaneously presented at the point-symmetrical position in the nonassociated visual field quadrant. The result makes a convincing case that the contextual effects involve feedback from higher areas, because there are no direct callosal connections that allow such interhemispheric contextual modulation. This enhancement from the ipsilateral hemifield may help rapid position-and-size-invariant detection of a circular pattern, which may be special among visual structures because of its ubiquity in natural scenes. Early visual areas as well as higher ones may play a more essential role in perceiving the unity of the real world than previously thought.

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.

Integration of texture and disparity cues to surface slant in dorsal visual cortex.

Reliable estimation of three-dimensional (3D) surface orientation is critical for recognizing and interacting with complex 3D objects in our environment. Human observers maximize the reliability of their estimates of surface slant by integrating multiple depth cues. Texture and binocular disparity are two such cues, but they are qualitatively very different. Existing evidence suggests that representations of surface tilt from each of these cues coincide at the single-neuron level in higher cortical areas. However, the cortical circuits responsible for 1) integration of such qualitatively distinct cues and 2) encoding the slant component of surface orientation have not been assessed. We tested for cortical responses related to slanted plane stimuli that were defined independently by texture, disparity, and combinations of these two cues. We analyzed the discriminability of functional MRI responses to two slant angles using multivariate pattern classification. Responses in visual area V3B/KO to stimuli containing congruent cues were more discriminable than those elicited by single cues, in line with predictions based on the fusion of slant estimates from component cues. This improvement was specific to congruent combinations of cues: incongruent cues yielded lower decoding accuracies, which suggests the robust use of individual cues in cases of large cue conflicts. These data suggest that area V3B/KO is intricately involved in the integration of qualitatively dissimilar depth cues.

Late development of cue integration is linked to sensory fusion in cortex.

Summary Adults optimize perceptual judgements by integrating different types of sensory information [1, 2]. This engages specialized neural circuits that fuse signals from the same [3, 4, 5] or different [6] modalities. Whereas young children can use sensory cues independently, adult-like precision gains from cue combination only emerge around ages 10 to 11 years [7, 8, 9]. Why does it take so long to make best use of sensory information? Existing data cannot distinguish whether this (1) reflects surprisingly late changes in sensory processing (sensory integration mechanisms in the brain are still developing) or (2) depends on post-perceptual changes (integration in sensory cortex is adult-like, but higher-level decision processes do not access the information) [10]. We tested visual depth cue integration in the developing brain to distinguish these possibilities. We presented children aged 6–12 years with displays depicting depth from binocular disparity and relative motion and made measurements using psychophysics, retinotopic mapping, and pattern classification fMRI. Older children (>10.5 years) showed clear evidence for sensory fusion in V3B, a visual area thought to integrate depth cues in the adult brain [3, 4, 5]. By contrast, in younger children (<10.5 years), there was no evidence for sensory fusion in any visual area. This significant age difference was paired with a shift in perceptual performance around ages 10 to 11 years and could not be explained by motion artifacts, visual attention, or signal quality differences. Thus, whereas many basic visual processes mature early in childhood [11, 12], the brain circuits that fuse cues take a very long time to develop.

Perceptual integration for qualitatively different 3-d cues in the human brain

The visual systems flexibility in estimating depth is remarkable: We readily perceive 3-D structure under diverse conditions from the seemingly random dots of a “magic eye” stereogram to the aesthetically beautiful, but obviously flat, canvasses of the Old Masters. Yet, 3-D perception is often enhanced when different cues specify the same depth. This perceptual process is understood as Bayesian inference that improves sensory estimates. Despite considerable behavioral support for this theory, insights into the cortical circuits involved are limited. Moreover, extant work tested quantitatively similar cues, reducing some of the challenges associated with integrating computationally and qualitatively different signals. Here we address this challenge by measuring fMRI responses to depth structures defined by shading, binocular disparity, and their combination. We quantified information about depth configurations (convex “bumps” vs. concave “dimples”) in different visual cortical areas using pattern classification analysis. We found that fMRI responses in dorsal visual area V3B/KO were more discriminable when disparity and shading concurrently signaled depth, in line with the predictions of cue integration. Importantly, by relating fMRI and psychophysical tests of integration, we observed a close association between depth judgments and activity in this area. Finally, using a cross-cue transfer test, we found that fMRI responses evoked by one cue afford classification of responses evoked by the other. This reveals a generalized depth representation in dorsal visual cortex that combines qualitatively different information in line with 3-D perception.

fMRI evidence for areas that process surface gloss in the human visual cortex.

Highlights • Glossiness information is mainly processed along ventral visual pathway.• The posterior fusiform sulcus (pFs) is especially selective to surface gloss.• V3B/KO responds to gloss, but differentially from the pFs.

Neocortical Rebound Depolarization Enhances Visual Perception

Animals are constantly exposed to the time-varying visual world. Because visual perception is modulated by immediately prior visual experience, visual cortical neurons may register recent visual history into a specific form of offline activity and link it to later visual input. To examine how preceding visual inputs interact with upcoming information at the single neuron level, we designed a simple stimulation protocol in which a brief, orientated flashing stimulus was subsequently coupled to visual stimuli with identical or different features. Using in vivo whole-cell patch-clamp recording and functional two-photon calcium imaging from the primary visual cortex (V1) of awake mice, we discovered that a flash of sinusoidal grating per se induces an early, transient activation as well as a long-delayed reactivation in V1 neurons. This late response, which started hundreds of milliseconds after the flash and persisted for approximately 2 s, was also observed in human V1 electroencephalogram. When another drifting grating stimulus arrived during the late response, the V1 neurons exhibited a sublinear, but apparently increased response, especially to the same grating orientation. In behavioral tests of mice and humans, the flashing stimulation enhanced the detection power of the identically orientated visual stimulation only when the second stimulation was presented during the time window of the late response. Therefore, V1 late responses likely provide a neural basis for admixing temporally separated stimuli and extracting identical features in time-varying visual environments.

fMRI Analysis-by-Synthesis Reveals a Dorsal Hierarchy That Extracts Surface Slant

The brains skill in estimating the 3-D orientation of viewed surfaces supports a range of behaviors, from placing an object on a nearby table, to planning the best route when hill walking. This ability relies on integrating depth signals across extensive regions of space that exceed the receptive fields of early sensory neurons. Although hierarchical selection and pooling is central to understanding of the ventral visual pathway, the successive operations in the dorsal stream are poorly understood. Here we use computational modeling of human fMRI signals to probe the computations that extract 3-D surface orientation from binocular disparity. To understand how representations evolve across the hierarchy, we developed an inference approach using a series of generative models to explain the empirical fMRI data in different cortical areas. Specifically, we simulated the responses of candidate visual processing algorithms and tested how well they explained fMRI responses. Thereby we demonstrate a hierarchical refinement of visual representations moving from the representation of edges and figure–ground segmentation (V1, V2) to spatially extensive disparity gradients in V3A. We show that responses in V3A are little affected by low-level image covariates, and have a partial tolerance to the overall depth position. Finally, we show that responses in V3A parallel perceptual judgments of slant. This reveals a relatively short computational hierarchy that captures key information about the 3-D structure of nearby surfaces, and more generally demonstrates an analysis approach that may be of merit in a diverse range of brain imaging domains.

Cortical and subcortical responses to biological motion

ABSTRACT Using fMRI and multivariate analyses we sought to understand the neural representations of articulated body shape and local kinematics in biological motion. We show that in addition to a cortical network that includes areas identified previously for biological motion perception, including the posterior superior temporal sulcus, inferior frontal gyrus, and ventral body areas, the ventral lateral nucleus, a presumably motoric thalamic area is sensitive to both form and kinematic information in biological motion. Our findings suggest that biological motion perception is not achieved as an end‐point of segregated cortical form and motion networks as often suggested, but instead involves earlier parts in the visual system including a subcortical network. HIGHLIGHTSBiological motion perception implicates both form‐based and kinematic processes.We used fMRI to examine neural responses to biological motion.Form and kinematics information are reflected widely in cortex.A presumably motoric thalamic nucleus (VLN) also responds to biological motion.