Cortical Reorganization of Peripheral Vision Induced by Simulated Central Vision Loss.

When one's central vision is deprived, a spared part of the peripheral retina acts as a pseudofovea for fixation. The neural mechanisms underlying this compensatory adjustment remain unclear. Here we report cortical reorganization induced by simulated central vision loss. Human subjects of both sexes learned to place the target at an eccentric retinal locus outside their blocked visual field for object tracking. Before and after training, we measured visual crowding-a bottleneck of object identification in peripheral vision, using psychophysics and fMRI. We found that training led to an axis-specific reduction of crowding. The change of the crowding effect was reflected in the change of BOLD signal, as a release of cortical suppression in multiple visual areas starting as early as V1. Our findings suggest that the adult visual system is capable of reshaping its oculomotor control and sensory coding to adapt to impoverished visual input.SIGNIFICANCE STATEMENT By simulating central vision loss in normally sighted adults, we found that oculomotor training not only induces PRL, but also facilitates form processing in peripheral vision. As subjects learned to place the target at an eccentric retinal locus, "visual crowding"-the detrimental effect of clutter on peripheral object identification-was reduced. The reduction of the crowding effect was accompanied by a release of response suppression in the visual cortex. These findings indicate that the adult visual system is capable of reshaping the peripheral vision to adapt to central vision loss.

Contextual-Dependent Attention Effect on Crowded Orientation Signals in Human Visual Cortex.

A target becomes hard to identify with nearby visual stimuli. This phenomenon, known as crowding, places a fundamental limit on conscious perception and object recognition. To understand the neural representation of crowded stimuli, we used fMRI and a forward encoding model to reconstruct the target-specific feature from multivoxel activation patterns evoked by orientation patches. Orientation-selective response profiles were constructed in V1-V4 for a target embedded in different contexts. Subjects of both sexes either directed their attention over all the orientation patches or selectively to the target. In the context with a weak crowding effect, attending to the target enhanced the orientation selectivity of the response profile; such effect increased along the visual pathway. In the context with a strong crowding effect, attending to the target enhanced the orientation selectivity of the response profile in the earlier visual area, but not in V4. The increase and decrease of orientation selectivity along the visual hierarchy demonstrate a contextual-dependent attention effect on crowded orientation signals: in the context with a weak crowding effect, selective attention gradually resolves the target from nearby distractors along the hierarchy; in the context with a strong crowding effect, while selective attention maintains the target feature in the earlier visual area, its effect decreases in the downstream area. Our findings reveal how the human visual system represents the target-specific feature at multiple stages under the limit of attention selection in a cluttered scene.SIGNIFICANCE STATEMENT Using fMRI and a forward encoding model, we reconstructed orientation-selective response profiles for a target embedded in crowded contexts. In the context with a weak crowding effect, attention gradually resolves the target from nearby distractors along the visual hierarchy. In the context with a strong crowding effect, while the feature of the target is preserved in the early visual cortex, it degrades in the later visual processing stage. The increase and decrease of orientation selectivity along the visual hierarchy reveal how the human visual system strikes to present the target-specific feature under the limit of attention selection in a cluttered scene.

Hemifield columns co-opt ocular dominance column structure in human achiasma.

In the absence of an optic chiasm, visual input to the right eye is represented in primary visual cortex (V1) in the right hemisphere, while visual input to the left eye activates V1 in the left hemisphere. Retinotopic mapping In V1 reveals that in each hemisphere left and right visual hemifield representations are overlaid (Hoffmann et al., 2012). To explain how overlapping hemifield representations in V1 do not impair vision, we tested the hypothesis that visual projections from nasal and temporal retina create interdigitated left and right visual hemifield representations in V1, similar to the ocular dominance columns observed in neurotypical subjects (Victor et al., 2000). We used high-resolution fMRI at 7T to measure the spatial distribution of responses to left- and right-hemifield stimulation in one achiasmic subject. T2-weighted 2D Spin Echo images were acquired at 0.8mm isotropic resolution. The left eye was occluded. To the right eye, a presentation of flickering checkerboards alternated between the left and right visual fields in a blocked stimulus design. The participant performed a demanding orientation-discrimination task at fixation. A general linear model was used to estimate the preference of voxels in V1 to left- and right-hemifield stimulation. The spatial distribution of voxels with significant preference for each hemifield showed interdigitated clusters which densely packed V1 in the right hemisphere. The spatial distribution of hemifield-preference voxels in the achiasmic subject was stable between two days of testing and comparable in scale to that of human ocular dominance columns. These results are the first in vivo evidence showing that visual hemifield representations interdigitate in achiasmic V1 following a similar developmental course to that of ocular dominance columns in V1 with intact optic chiasm.

What Is Actually Affected by the Scrambling of Objects When Localizing the Lateral Occipital Complex?

The lateral occipital complex (LOC), the cortical region critical for shape perception, is localized with fMRI by its greater BOLD activity when viewing intact objects compared with their scrambled versions (resembling texture). Despite hundreds of studies investigating LOC, what the LOC localizer accomplishes-beyond distinguishing shape from texture-has never been resolved. By independently scattering the intact parts of objects, the axis structure defining the relations between parts was no longer defined. This led to a diminished BOLD response, despite the increase in the number of independent entities (the parts) produced by the scattering, thus indicating that LOC specifies interpart relations, in addition to specifying the shape of the parts themselves. LOC's sensitivity to relations is not confined to those between parts but is also readily apparent between objects, rendering it-and not subsequent "place" areas-as the critical region for the representation of scenes. Moreover, that these effects are witnessed with novel as well as familiar intact objects and scenes suggests that the relations are computed on the fly, rather than being retrieved from memory.

Human efficiency in detecting and discriminating biological motion.

Using an "information meter" provided by ideal observer analysis, we measured the efficiency with which human observers processed different walking stimuli against luminance noise and spatial uncertainty to either detect the presence of a walker or to discriminate the walking direction. Human efficiency was examined across four renderings of a human walker: contour, point lights, silhouette, and skeleton. We replicated the previous finding of low discrimination efficiency in biological motion (Gold, Tadin, Cook, & Blake, 2008) and also found low detection efficiency for biological motion. Interestingly, in both detection and discrimination tasks, the skeleton display was among those yielding the highest level of efficiency in processing visual information. This finding suggests that structural information about the relative position of joints, highlighted in the skeleton display, provides a critical component of the internal representation for biological motion.

Crowding, visual awareness, and their respective neural loci.

In peripheral vision, object identification can be impeded when a target object is flanked by other objects. This phenomenon of crowding has been attributed to basic processes associated with image encoding by the visual system, but the neural origin of crowding is not known. Determining whether crowding depends on subjective awareness of the flankers can provide information on the neural origin of crowding. However, recent studies that manipulated flanker awareness have yielded conflicting results. In the current study, we suppressed flanker awareness with two methods: interocular suppression (IOS) and adaptation-induced blindness (AIB). We tested two different types of stimuli: gratings and letters. With IOS, we found that the magnitude of crowding increased as the number of physical flankers increased, even when the observers did not report seeing any of the flankers. In contrast, when flanker awareness was manipulated with AIB, the magnitude of crowding increased with the number of perceived flankers. Our results show that whether crowding is contingent on awareness of the flankers depends on the method used to suppress awareness. In addition, our results imply that the locus of crowding is upstream from the neural locus of IOS and close to or downstream from that of AIB. Neurophysiology and neuroimaging studies jointly implicate mid-to-high level visual processing stages for IOS, while direct evidence regarding the neural locus of AIB is limited. The most consistent interpretation of our empirical findings is to place the neural locus of crowding at an early cortical site, such as V1 or V2.

Object crowding in age-related macular degeneration.

Crowding, the phenomenon of impeded object identification due to clutter, is believed to be a key limiting factor of form vision in the peripheral visual field. The present study provides a characterization of object crowding in age-related macular degeneration (AMD) measured at the participants' respective preferred retinal loci with binocular viewing. Crowding was also measured in young and age-matched controls at the same retinal locations, using a fixation-contingent display paradigm to allow unlimited stimulus duration. With objects, the critical spacing of crowding for AMD participants was not substantially different from controls. However, baseline contrast energy thresholds in the noncrowded condition were four times that of the controls. Crowding further exacerbated deficits in contrast sensitivity to three times the normal crowding-induced contrast energy threshold elevation. These findings indicate that contrast-sensitivity deficit is a major limiting factor of object recognition for individuals with AMD, in addition to crowding. Focusing on this more tractable deficit of AMD may lead to more effective remediation and technological assistance.

Automated retinofugal visual pathway reconstruction with multi-shell HARDI and FOD-based analysis.

Diffusion MRI tractography provides a non-invasive modality to examine the human retinofugal projection, which consists of the optic nerves, optic chiasm, optic tracts, the lateral geniculate nuclei (LGN) and the optic radiations. However, the pathway has several anatomic features that make it particularly challenging to study with tractography, including its location near blood vessels and bone-air interface at the base of the cerebrum, crossing fibers at the chiasm, somewhat-tortuous course around the temporal horn via Meyer's Loop, and multiple closely neighboring fiber bundles. To date, these unique complexities of the visual pathway have impeded the development of a robust and automated reconstruction method using tractography. To overcome these challenges, we develop a novel, fully automated system to reconstruct the retinofugal visual pathway from high-resolution diffusion imaging data. Using multi-shell, high angular resolution diffusion imaging (HARDI) data, we reconstruct precise fiber orientation distributions (FODs) with high order spherical harmonics (SPHARM) to resolve fiber crossings, which allows the tractography algorithm to successfully navigate the complicated anatomy surrounding the retinofugal pathway. We also develop automated algorithms for the identification of ROIs used for fiber bundle reconstruction. In particular, we develop a novel approach to extract the LGN region of interest (ROI) based on intrinsic shape analysis of a fiber bundle computed from a seed region at the optic chiasm to a target at the primary visual cortex. By combining automatically identified ROIs and FOD-based tractography, we obtain a fully automated system to compute the main components of the retinofugal pathway, including the optic tract and the optic radiation. We apply our method to the multi-shell HARDI data of 215 subjects from the Human Connectome Project (HCP). Through comparisons with post-mortem dissection measurements, we demonstrate the retinotopic organization of the optic radiation including a successful reconstruction of Meyer's loop. Then, using the reconstructed optic radiation bundle from the HCP cohort, we construct a probabilistic atlas and demonstrate its consistency with a post-mortem atlas. Finally, we generate a shape-based representation of the optic radiation for morphometry analysis.

The Lateral Occipital Complex shows no net response to object familiarity.

In 1995, Malach et al. discovered an area whose fMRI BOLD response was greater when viewing intact, familiar objects than when viewing their scrambled versions (resembling texture). Since then hundreds of studies have explored this late visual region termed the Lateral Occipital Complex (LOC), which is now known to be critical for shape perception (James, Culham, Humphrey, Milner, & Goodale, 2003). Malach et al. (1995) discounted a role of familiarity by showing that "abstract" Henry Moore sculptures, unfamiliar to the subjects, also activated this region. This characterization of LOC as a region that responds to shape independently of familiarity has been accepted but never tested with control of the same low-level features. We assessed LOC's response to objects that had identical parts in two different arrangements, one familiar and the other novel. Malach was correct: There is no net effect of familiarity in LOC. However, a multivoxel correlation analysis showed that LOC does distinguish familiar from novel objects.

Visual crowding in V1.

In peripheral vision, objects in clutter are difficult to identify. The exact cause of this "crowding" effect is unclear. To perceive coherent shapes in clutter, the visual system must integrate certain local features across receptive fields while preventing others from being combined. It is believed that this selective feature integration-segmentation process is impaired in peripheral vision, leading to crowding. We used functional magnetic resonance imaging (fMRI) to investigate the neural origin of crowding. We found that crowding was associated with suppressed fMRI signal as early as V1, regardless of whether attention was directed toward or away from a target stimulus. This suppression in early visual cortex was greatest for stimuli that produced the strongest crowding. In contrast, the pattern of activity was mixed in higher level visual areas, such as the lateral occipital cortex. These results support the view that the deficiency in feature integration and segmentation in peripheral vision is present at the earliest stages of cortical processing.

Radial-tangential anisotropy of crowding in the early visual areas.

Crowding, the inability to recognize an individual object in clutter (Bouma H. Nature 226: 177-178, 1970), is considered a major impediment to object recognition in peripheral vision. Despite its significance, the cortical loci of crowding are not well understood. In particular, the role of the primary visual cortex (V1) remains unclear. Here we utilize a diagnostic feature of crowding to identify the earliest cortical locus of crowding. Controlling for other factors, radially arranged flankers induce more crowding than tangentially arranged ones (Toet A, Levi DM. Vision Res 32: 1349-1357, 1992). We used functional magnetic resonance imaging (fMRI) to measure the change in mean blood oxygenation level-dependent (BOLD) response due to the addition of a middle letter between a pair of radially or tangentially arranged flankers. Consistent with the previous finding that crowding is associated with a reduced BOLD response [Millin R, Arman AC, Chung ST, Tjan BS. Cereb Cortex (July 5, 2013). doi:10.1093/cercor/bht159], we found that the BOLD signal evoked by the middle letter depended on the arrangement of the flankers: less BOLD response was associated with adding the middle letter between radially arranged flankers compared with adding it between tangentially arranged flankers. This anisotropy in BOLD response was present as early as V1 and remained significant in downstream areas. The effect was observed while subjects' attention was diverted away from the testing stimuli. Contrast detection threshold for the middle letter was unaffected by flanker arrangement, ruling out surround suppression of contrast response as a major factor in the observed BOLD anisotropy. Our findings support the view that V1 contributes to crowding.

A visual or tactile signal makes auditory speech detection more efficient by reducing uncertainty.

Acoustic speech is easier to detect in noise when the talker can be seen. This finding could be explained by integration of multisensory inputs or refinement of auditory processing from visual guidance. In two experiments, we studied two-interval forced-choice detection of an auditory 'ba' in acoustic noise, paired with various visual and tactile stimuli that were identically presented in the two observation intervals. Detection thresholds were reduced under the multisensory conditions vs. the auditory-only condition, even though the visual and/or tactile stimuli alone could not inform the correct response. Results were analysed relative to an ideal observer for which intrinsic (internal) noise and efficiency were independent contributors to detection sensitivity. Across experiments, intrinsic noise was unaffected by the multisensory stimuli, arguing against the merging (integrating) of multisensory inputs into a unitary speech signal, but sampling efficiency was increased to varying degrees, supporting refinement of knowledge about the auditory stimulus. The steepness of the psychometric functions decreased with increasing sampling efficiency, suggesting that the 'task-irrelevant' visual and tactile stimuli reduced uncertainty about the acoustic signal. Visible speech was not superior for enhancing auditory speech detection. Our results reject multisensory neuronal integration and speech-specific neural processing as explanations for the enhanced auditory speech detection under noisy conditions. Instead, they support a more rudimentary form of multisensory interaction: the otherwise task-irrelevant sensory systems inform the auditory system about when to listen.

The perception of a face is no more than the sum of its parts.

When you see a person's face, how do you go about combining his or her facial features to make a decision about who that person is? Most current theories of face perception assert that the ability to recognize a human face is not simply the result of an independent analysis of individual features, but instead involves a holistic coding of the relationships among features. This coding is thought to enhance people's ability to recognize a face beyond what would be expected if each feature were shown in isolation. In the study reported here, we explicitly tested this idea by comparing human performance on facial-feature integration with that of an optimal Bayesian integrator. Contrary to the predictions of most current notions of face perception, our findings showed that human observers integrate facial features in a manner that is no better than would be predicted by their ability to use each individual feature when shown in isolation. That is, a face is perceived no better than the sum of its individual parts.

Contour enhancement benefits older adults with simulated central field loss.

PURPOSE: Age-related macular degeneration is the leading cause of vision loss among Americans aged >65 years. Currently, no effective treatment can reverse the central vision loss associated with most age-related macular degeneration. Digital image-processing techniques have been developed to improve image visibility for peripheral vision; however, both the selection and efficacy of such methods are limited. Progress has been difficult for two reasons: the exact nature of image enhancement that might benefit peripheral vision is not well understood, and efficient methods for testing such techniques have been elusive. The current study aims to develop both an effective image enhancement technique for peripheral vision and an efficient means for validating the technique. METHODS: We used a novel contour-detection algorithm to locate shape-defining edges in images based on natural-image statistics. We then enhanced the scene by locally boosting the luminance contrast along such contours. Using a gaze-contingent display, we simulated central visual field loss in normally sighted young (aged 18-30 years) and older adults (aged 58-88 years). Visual search performance was measured as a function of contour enhancement strength ["original" (unenhanced), "medium," and "high"]. For preference task, a separate group of subjects judged which image in a pair "would lead to better search performance." RESULTS: We found that although contour enhancement had no significant effect on search time and accuracy in young adults, Medium enhancement resulted in significantly shorter search time in older adults (about 13% reduction relative to original). Both age-groups preferred images with Medium enhancement over original (2-7 times). Furthermore, across age-groups, image content types, and enhancement strengths, there was a robust correlation between preference and performance. CONCLUSIONS: Our findings demonstrate a beneficial role of contour enhancement in peripheral vision for older adults. Our findings further suggest that task-specific preference judgments can be an efficient surrogate for performance testing.

Attention extracts signal in external noise: a BOLD fMRI study.

On the basis of results from behavioral studies that spatial attention improves the exclusion of external noise in the target region, we predicted that attending to a spatial region would reduce the impact of external noise on the BOLD response in corresponding cortical areas, seen as reduced BOLD responses in conditions with large amounts of external noise but relatively low signal, and increased dynamic range of the BOLD response to variations in signal contrast. We found that, in the presence of external noise, covert attention reduced the trial-by-trial BOLD response by 15.5-18.9% in low signal contrast conditions in V1. It also increased the BOLD dynamic range in V1, V2, V3, V3A/B, and V4 by a factor of at least three. Overall, covert attention reduced the impact of external noise by about 73-85% in these early visual areas. It also increased the contrast gain by a factor of 2.6-3.8.

Blood oxygenation level-dependent contrast response functions identify mechanisms of covert attention in early visual areas.

Covert attention can lead to improved performance in perceptual tasks. The neural and functional mechanisms of covert attention are still under investigation. Using both rapid event-related and mixed designs, we measured the blood oxygenation level-dependent functional MRI contrast response functions over the full range of contrast (0-100%) in the retinotopically defined early visual areas (V1, V2, V3, V3A, and V4) in humans. Covert attention increased both the baseline activities and contrast gains in the five cortical areas. The effect on baseline can be decomposed into a transient trial-by-trial component and a component across an entire attention block. On average, increase in contrast gain accounted for approximately 88.0%, 28.5%, 12.7%, 35.9%, and 25.2% of the trial-by-trial effects of attention in the five areas, respectively, and 22.2%, 12.8%, 7.4%, 19.7%, and 17.3% of the total effects of attention in those areas, consistent with single-unit findings in V4 and MT. The results provide strong evidence for a stimulus enhancement mechanism of attention as demonstrated in various behavioral studies.

Object crowding.

Crowding occurs when stimuli in the peripheral fields become harder to identify when flanked by other items. This phenomenon has been demonstrated extensively with simple patterns (e.g., Gabors and letters). Here, we characterize crowding for everyday objects. We presented three-item arrays of objects and letters, arranged radially and tangentially in the lower visual field. Observers identified the central target, and we measured contrast energy thresholds as a function of target-to-flanker spacing. Object crowding was similar to letter crowding in spatial extent but was much weaker. The average elevation in threshold contrast energy was in the order of 1 log unit for objects as compared to 2 log units for letters and silhouette objects. Furthermore, we examined whether the exterior and interior features of an object are differentially affected by crowding. We used a circular aperture to present or exclude the object interior. Critical spacings for these aperture and "donut" objects were similar to those of intact objects. Taken together, these findings suggest that crowding between letters and objects are essentially due to the same mechanism, which affects equally the interior and exterior features of an object. However, for objects defined with varying shades of gray, it is much easier to overcome crowding by increasing contrast.

Ideal observer analysis of crowding and the reduction of crowding through learning.

Crowding is a prominent phenomenon in peripheral vision where nearby objects impede one's ability to identify a target of interest. The precise mechanism of crowding is not known. We used ideal observer analysis and a noise-masking paradigm to identify the functional mechanism of crowding. We tested letter identification in the periphery with and without flanking letters and found that crowding increases equivalent input noise and decreases sampling efficiency. Crowding effectively causes the signal from the target to be noisier and at the same time reduces the visual system's ability to make use of a noisy signal. After practicing identification of flanked letters without noise in the periphery for 6 days, subjects' performance for identifying flanked letters improved (reduction of crowding). Across subjects, the improvement was attributable to either a decrease in crowding-induced equivalent input noise or an increase in sampling efficiency, but seldom both. This pattern of results is consistent with a simple model whereby learning reduces crowding by adjusting the spatial extent of a perceptual window used to gather relevant input features. Following learning, subjects with inappropriately large windows reduced their window sizes; while subjects with inappropriately small windows increased their window sizes. The improvement in equivalent input noise and sampling efficiency persists for at least 6 months.

Spatial-frequency and contrast properties of reading in central and peripheral vision.

In this study, we examined the effects of contrast and spatial frequency on reading speed and compared these effects between the normal fovea and periphery. We found that when text contrast was low, reading speed demonstrated spatial-frequency tuning properties, with a peak tuning frequency that partially scaled with print size. The spatial-frequency tuning disappeared when text contrast was 100%. The spatial-frequency tuning and scaling properties for reading were largely similar between the fovea and the periphery, and closely matched those for letter identification. Just as for the task of letter identification, we showed through an ideal-observer analysis that the spatial-frequency properties for reading could be primarily accounted for by the physical properties of the word stimuli combined with human observers' contrast sensitivity functions.

Efficient integration across spatial frequencies for letter identification in foveal and peripheral vision.

Objects in natural scenes are spatially broadband; in contrast, feature detectors in the early stages of visual processing are narrowly tuned in spatial frequency. Earlier studies of feature integration using gratings suggested that integration across spatial frequencies is suboptimal. Here we re-examined this conclusion using a letter identification task at the fovea and at 10 deg in the lower visual field. We found that integration across narrow-band (1-octave) spatial frequency components of letter stimuli is optimal in the fovea. Surprisingly, this optimality is preserved in the periphery, even though feature integration is known to be deficient in the periphery from studies of other form-vision tasks such as crowding. A model that is otherwise a white-noise ideal observer except for a limited spatial resolution defined by the human contrast sensitivity function and using internal templates slightly wider in bandwidth than the stimuli is able to account for the human data. Our findings suggest that deficiency in feature integration found in peripheral vision is not across spatial frequencies.