Faculty Bibliography

The visual system exploits multiple signals, including monocular and binocular cues, to determine the motion of objects through depth. In the laboratory, sensitivity to different three-dimensional (3D) motion cues varies across observers and is often weak for binocular cues. However, laboratory assessments may reflect factors beyond inherent perceptual sensitivity. For example, the appearance of weak binocular sensitivity may relate to extensive prior experience with two-dimensional (2D) displays in which binocular cues are not informative. Here we evaluated the impact of experience on motion-in-depth (MID) sensitivity in a virtual reality (VR) environment. We tested a large cohort of observers who reported having no prior VR experience and found that binocular cue sensitivity was substantially weaker than monocular cue sensitivity. As expected, sensitivity was greater when monocular and binocular cues were presented together than in isolation. Surprisingly, the addition of motion parallax signals appeared to cause observers to rely almost exclusively on monocular cues. As observers gained experience in the VR task, sensitivity to monocular and binocular cues increased. Notably, most observers were unable to distinguish the direction of MID based on binocular cues above chance level when tested early in the experiment, whereas most showed statistically significant sensitivity to binocular cues when tested late in the experiment. This result suggests that observers may discount binocular cues when they are first encountered in a VR environment. Laboratory assessments may thus underestimate the sensitivity of inexperienced observers to MID, especially for binocular cues.

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.

PURPOSE:To link optic nerve (ON) structural properties to clinical markers of glaucoma using advanced, semi-automated diffusion magnetic resonance imaging (dMRI) tractography in human glaucoma patients. METHODS:We characterized optic neuropathy in patients with unilateral advanced-stage glaucoma (n = 6) using probabilistic dMRI tractography and compared their results to those in healthy controls (n = 6). RESULTS:We successfully identified the ONs of glaucoma patients based on dMRI in all patients and confirmed that dMRI measures of the ONs correlated with clinical markers of glaucoma severity. Specifically, we found reduced fractional anisotropy (FA) in the ONs of eyes with advanced, as compared to mild, glaucoma (F(1,10) = 55.474, p < 0.0001, FDR < 0.0005). Furthermore, by comparing the ratios of ON FA in glaucoma patients to those of healthy controls (n = 6), we determined that this difference was beyond that expected from normal anatomical variation (F(1,9) = 20.276, p < 0. 005). Finally, we linked the dMRI measures of ON FA to standard clinical glaucoma measures. ON vertical cup-to-disc ratio (vCD) predicted ON FA (F(1,10) = 11.061, p < 0.01, R2 = 0.66), retinal nerve fiber layer thickness (RNFL) predicted ON FA (F(1,10) = 11.477, p < 0.01, R2 = 0.63) and ON FA predicted perceptual deficits (visual field index [VFI]) (F(1,10) = 15.308, p < 0.005, R2 = 0.52). CONCLUSION:We describe semi-automated methods to detect glaucoma-related structural changes using dMRI and confirm that they correlate with clinical measures of glaucoma.

To see color, the human visual system combines the response of three types of cone cells in the retina-a compressive process that discards a significant amount of spectral information. Here, we present designs based on thin-film optical filters with the goal of enhancing human color vision by breaking its inherent binocular redundancy, providing different spectral content to each eye. We fabricated a set of optical filters that "splits" the response of the short-wavelength cone between the two eyes in individuals with typical trichromatic vision, simulating the presence of approximately four distinct cone types. Such an increase in the number of effective cone types can reduce the prevalence of metamers-pairs of distinct spectra that resolve to the same tristimulus values. This technique may result in an enhancement of spectral perception, with applications ranging from camouflage detection and anti-counterfeiting to new types of artwork and data visualization.

People make surprising but reliable perceptual errors. Here, we provide a unified explanation for systematic errors in the perception of three-dimensional (3-D) motion. To do so, we characterized the binocular retinal motion signals produced by objects moving through arbitrary locations in 3-D. Next, we developed a Bayesian model, treating 3-D motion perception as optimal inference given sensory noise in the measurement of retinal motion. The model predicts a set of systematic perceptual errors, which depend on stimulus distance, contrast, and eccentricity. We then used a virtual-reality headset as well as a standard 3-D desktop stereoscopic display to test these predictions in a series of perceptual experiments. As predicted, we found evidence that errors in 3-D motion perception depend on the contrast, viewing distance, and eccentricity of a stimulus. These errors include a lateral bias in perceived motion direction and a surprising tendency to misreport approaching motion as receding and vice versa. In sum, we present a Bayesian model that provides a parsimonious account for a range of systematic misperceptions of motion in naturalistic environments.

PURPOSE:Amblyopia is associated with a broad array of perceptual and neural abnormalities in the visual system, particularly in untreated or unsuccessfully treated populations. Traditionally, it has been believed that the neural abnormalities are confined to the visual cortex and subcortex (e.g., lateral geniculate nucleus). Here, we investigate the presence of neuroanatomical abnormalities earlier in the visual stream, in the optic nerves and tracts, of participants with two predominant forms of amblyopia. METHODS:We used diffusion magnetic resonance imaging and probabilistic tractography to compare the microstructural properties of five white matter visual pathways between 15 participants with amblyopia (eight anisometropic, five strabismic, and two exhibiting both etiologies), and 13 age-matched controls. RESULTS:Participants with amblyopia exhibited significantly smaller mean fractional anisotropy in the optic nerve and optic tract (0.26 and 0.31 vs. 0.31 and 0.36 in controls, respectively). We also found greater mean diffusivity in the optic radiation compared to controls (0.72 μm2/s vs. 0.68 μm2/s, respectively). Comparing etiologies, the abnormalities in the precortical pathways tended to be more severe in participants with anisometropic compared to strabismic amblyopia, and anisometropic participants' optic nerves, optic tracts, and optic radiations significantly differed from control participants' (all, P < 0.05). CONCLUSIONS:The results indicate that amblyopia may be associated with microstructural abnormalities in neural networks as early as the retina, and these abnormalities may differ between amblyopic etiologies.

3D motion perception is of central importance to daily life. However, when tested in laboratory settings, sensitivity to 3D motion signals is found to be poor, leading to the view that heuristics and prior assumptions are critical for 3D motion perception. Here we explore an alternative: sensitivity to 3D motion signals is context-dependent and must be learned based on explicit visual feedback in novel environments. The need for action-contingent visual feedback is well-established in the developmental literature. For example, young kittens that are passively moved through an environment, but unable to move through it themselves, fail to develop accurate depth perception. We find that these principles also obtain in adult human perception. Observers that do not experience visual consequences of their actions fail to develop accurate 3D motion perception in a virtual reality environment, even after prolonged exposure. By contrast, observers that experience the consequences of their actions improve performance based on available sensory cues to 3D motion. Specifically, we find that observers learn to exploit the small motion parallax cues provided by head jitter. Our findings advance understanding of human 3D motion processing and form a foundation for future study of perception in virtual and natural 3D environments.

Optimal functioning in everyday life requires the ability to override reflexive emotional responses and prevent affective spillover to situations or people unrelated to the source of emotion. In the current study, we investigated whether the lateral prefrontal cortex (lPFC) causally regulates the influence of emotional information on subsequent judgments. We disrupted left lPFC function using transcranial magnetic stimulation (TMS) and recorded electroencephalography (EEG) before and after. Subjects evaluated the likeability of novel neutral faces after a brief exposure to a happy or fearful face. We found that lPFC inhibition biased evaluations of novel faces according to the previously processed emotional expression. Greater frontal EEG alpha power, reflecting increased inhibition by TMS, predicted increased behavioral bias. TMS-induced affective misattribution was long-lasting: Emotionally biased first impressions formed during lPFC inhibition were still detectable outside of the laboratory 3 days later. These findings indicate that lPFC serves an important emotion-regulation function by preventing incidental emotional encoding from automatically biasing subsequent appraisals.

Conscious awareness of negative cues is thought to enhance emotion-regulatory capacity, but the neural mechanisms underlying this effect are unknown. Using continuous flash suppression (CFS) in the MRI scanner, we manipulated visual awareness of fearful faces during an affect misattribution paradigm, in which preferences for neutral objects can be biased by the valence of a previously presented stimulus. The amygdala responded to fearful faces independently of awareness. However, when awareness of fearful faces was prevented, individuals with greater amygdala responses displayed a negative bias toward unrelated novel neutral faces. In contrast, during the aware condition, inverse coupling between the amygdala and prefrontal cortex reduced this bias, particularly among individuals with higher structural connectivity in the major white matter pathway connecting the prefrontal cortex and amygdala. Collectively, these results indicate that awareness promotes the function of a critical emotion-regulatory network targeting the amygdala, providing a mechanistic account for the role of awareness in emotion regulation.