Faculty Bibliography

The visual system develops abnormally when visual input is absent or degraded during a critical period early in life. Restoration of the visual input later in life is generally thought to have limited benefit because the visual system will lack sufficient plasticity to adapt to and utilize the information from the eyes. Recent evidence, however, shows that congenitally blind adolescents can recover both low-level and higher-level visual function following surgery. In this study, we assessed behavioral performance in both a visual acuity and a face perception task alongside longitudinal structural white matter changes in terms of fractional anisotropy (FA) and mean diffusivity (MD). We studied congenitally blind patients with dense bilateral cataracts, who received cataract surgery at different stages of adolescence. Our goal was to differentiate between age- and surgery-related changes in both behavioral performance and structural measures to identify neural correlates which might contribute to recovery of visual function. We observed surgery-related long-term increases of structural integrity of late-visual pathways connecting the occipital regions with ipsilateral fronto-parieto-temporal regions or homotopic contralateral areas. Comparison to a group of age-matched healthy participants indicated that these improvements went beyond the expected changes in FA and MD based on maturation alone. Finally, we found that the extent of behavioral improvement in face perception was mediated by changes in structural integrity in late visual pathways. Our results suggest that sufficient plasticity remains in adolescence to partially overcome abnormal visual development and help localize the sites of neural change underlying sight recovery.

Accurate motion perception requires that the visual system integrate the 2D retinal motion signals received by the two eyes into a single representation of 3D motion. However, most experimental paradigms present the same stimulus to the two eyes, signaling motion limited to a 2D fronto-parallel plane. Such paradigms are unable to dissociate the representation of 3D head-centric motion signals (i.e., 3D object motion relative to the observer) from the associated 2D retinal motion signals. Here, we used stereoscopic displays to present separate motion signals to the two eyes and examined their representation in visual cortex using fMRI. Specifically, we presented random-dot motion stimuli that specified various 3D head-centric motion directions. We also presented control stimuli, which matched the motion energy of the retinal signals, but were inconsistent with any 3D motion direction. We decoded motion direction from BOLD activity using a probabilistic decoding algorithm. We found that 3D motion direction signals can be reliably decoded in three major clusters in the human visual system. Critically, in early visual cortex (V1-V3), we found no significant difference in decoding performance between stimuli specifying 3D motion directions and the control stimuli, suggesting that these areas represent the 2D retinal motion signals, rather than 3D head-centric motion itself. In voxels in and surrounding hMT and IPS0 however, decoding performance was consistently superior for stimuli that specified 3D motion directions compared to control stimuli. Our results reveal the parts of the visual processing hierarchy that are critical for the transformation of retinal into 3D head-centric motion signals and suggest a role for IPS0 in their representation, in addition to its sensitivity to 3D object structure and static depth.

The discriminability of motion direction is asymmetric, with some motion directions that are better discriminated than others. For example, discrimination of directions near the cardinal axes (upward/downward/leftward/rightward) tends to be better than oblique directions. Here, we tested discriminability for multiple motion directions at multiple polar angle locations. We found three systematic asymmetries. First, we found a large cardinal advantage in a cartesian reference frame - better discriminability for motion near cardinal reference directions than oblique directions. Second, we found a moderate cardinal advantage in a polar reference frame - better discriminability for motion near radial (inward/outward) and tangential (clockwise/counterclockwise) reference directions than other directions. Third, we found a small advantage for discriminating motion near radial compared to tangential reference directions. The three advantages combine in an approximately linear manner, and together predict variation in motion discrimination as a function of both motion direction and location around the visual field. For example, best performance is found for radial motion on the horizontal and vertical meridians, as these directions encompass all three advantages, whereas poorest performance is found for oblique motion stimuli located on the horizontal and vertical meridians, as these directions encompass all three disadvantages. Our results constrain models of motion perception and suggest that reference frames at multiple stages of the visual processing hierarchy limit performance.

A central question in neuroscience is how sensory inputs are transformed into percepts. At this point, it is clear that this process is strongly influenced by prior knowledge of the sensory environment. Bayesian ideal observer models provide a useful link between data and theory that can help researchers evaluate how prior knowledge is represented and integrated with incoming sensory information. However, the statistical prior employed by a Bayesian observer cannot be measured directly, and must instead be inferred from behavioral measurements. Here, we review the general problem of inferring priors from psychophysical data, and the simple solution that follows from assuming a prior that is a Gaussian probability distribution. As our understanding of sensory processing advances, however, there is an increasing need for methods to flexibly recover the shape of Bayesian priors that are not well approximated by elementary functions. To address this issue, we describe a novel approach that applies to arbitrary prior shapes, which we parameterize using mixtures of Gaussian distributions. After incorporating a simple approximation, this method produces an analytical solution for psychophysical quantities that can be numerically optimized to recover the shapes of Bayesian priors. This approach offers advantages in flexibility, while still providing an analytical framework for many scenarios. We provide a MATLAB toolbox implementing key computations described herein.

Robust 3-D visual perception is achieved by integrating stereoscopic and perspective cues. The canonical model describing the integration of these cues assumes that perspective signals sensed by the left and right eyes are indiscriminately pooled into a single representation that contributes to perception. Here, we show that this model fails to account for 3-D motion perception. We measured the sensitivity of male macaque monkeys to 3-D motion signaled by left-eye perspective cues, right-eye perspective cues, stereoscopic cues, and all three cues combined. The monkeys exhibited idiosyncratic differences in their biases and sensitivities for each cue, including left- and right-eye perspective cues, suggesting that the signals undergo at least partially separate neural processing. Importantly, sensitivity to combined cue stimuli was greater than predicted by the canonical model, which previous studies found to account for the perception of 3-D orientation in both humans and monkeys. Instead, 3-D motion sensitivity was best explained by a model in which stereoscopic cues were integrated with left- and right-eye perspective cues whose representations were at least partially independent. These results indicate that the integration of perspective and stereoscopic cues is a shared computational strategy across 3-D processing domains. However, they also reveal a fundamental difference in how left- and right-eye perspective signals are represented for 3-D orientation versus motion perception. This difference results in more effective use of available sensory information in the processing of 3-D motion than orientation and may reflect the temporal urgency of avoiding and intercepting moving objects.

Motion perception is a critical function of the visual system. In a three-dimensional environment, multiple sensory cues carry information about an object's motion trajectory. Previous work has quantified the contribution of binocular motion cues, such as interocular velocity differences and changing disparities over time, as well as monocular motion cues, such as size and density changes. However, even when these cues are presented in concert, observers will systematically misreport the direction of motion-in-depth. Although in the majority of laboratory experiments head position is held fixed using a chin or head rest, an observer's head position is subject to involuntary small movements under real-world viewing conditions. Here, we considered the potential impact of such "head jitter" on motion-in-depth perception. We presented visual stimuli in a head-mounted virtual reality device that facilitated low latency head tracking and asked observers to judge 3D object motion. We found performance improved when we updated the visual display consistent with the small changes in head position. When we disrupted or delayed head movement-contingent updating of the visual display, the proportion of motion-in-depth misreports again increased, reflected in both a reduction in sensitivity and an increase in bias. Our findings identify a critical function of head jitter in visual motion perception, which has been obscured in most (head-fixed and non-head jitter contingent) laboratory experiments.

Amblyopia is a common perceptual disorder resulting from abnormal visual input during development. The clinical presentation and visual deficits associated with amblyopia are well characterized. Less is known however, about amblyopia's impact on the central nervous system (CNS). While early insights into the neuropathophysiology of amblyopia have been based on findings from animal models and postmortem human studies, recent advances in noninvasive magnetic resonance imaging (MRI) techniques have enabled the study of amblyopia's effects in vivo. We review recent retinal and neuroimaging research documenting amblyopia's structural and functional impact on the CNS. Clinical imaging provides some evidence for retinal and optic nerve abnormalities in amblyopic eyes, although the overall picture remains inconclusive. Neuroimaging studies report clearer changes in both structure and function of the visual pathways. In the optic nerves, optic tracts, and optic radiations of individuals with amblyopia, white-matter integrity is decreased. In the lateral geniculate nuclei, gray matter volume is decreased and neural activity is reduced. Reduced responses are also seen in the amblyopic primary visual cortex and extrastriate areas. Overall, amblyopia impacts structure and function at multiple sites along the visual processing hierarchy. Moreover, there is some evidence that amblyopia's impact on the CNS depends on its etiology, with different patterns of results for strabismic and anisometropic amblyopia. To clarify the impact of amblyopia on the CNS, simultaneous collection of retinal, neural, and perceptual measures should be employed. Such an approach will help (1) distinguish cause and effect of amblyopic impairments, (2) separate the impact of amblyopia from other superimposed conditions, and (3) identify the importance of amblyopic etiology to specific neural and perceptual deficits.

Metacognitive awareness-the ability to know that one is having a particular experience-is thought to guide optimal behavior, but its neural bases continue to be the subject of vigorous debate. Prior work has identified correlations between perceptual metacognitive ability and the structure and function of lateral prefrontal cortex (LPFC); however, evidence for a causal role of this region in promoting metacognition is controversial. Moreover, whether LPFC function promotes metacognitive awareness of perceptual and emotional features of complex, yet ubiquitous face stimuli is unknown. Here, using model-based analyses following a causal intervention to LPFC in humans, we demonstrate that LPFC function promotes metacognitive awareness of the orientation of faces-although not of their emotional expressions. Collectively, these data support the causal involvement of the prefrontal cortex in metacognitive awareness, and indicate that the role of LPFC in metacognition encompasses perceptual experiences of naturalistic social stimuli.