White matter plasticity following cataract surgery in congenitally blind patients.

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.

Identifying cortical areas that underlie the transformation from 2D retinal to 3D head-centric motion signals.

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.

Task feedback suggests a post-perceptual component to serial dependence.

Decisions across a range of perceptual tasks are biased toward past stimuli. Such serial dependence is thought to be an adaptive low-level mechanism that promotes perceptual stability across time. However, recent studies suggest post-perceptual mechanisms may also contribute to serially biased responses, calling into question a single locus of serial dependence and the nature of integration of past and present sensory inputs. We measured serial dependence in the context of a three-dimensional (3D) motion perception task where uncertainty in the sensory information varied substantially from trial to trial. We found that serial dependence varied with stimulus properties that impact sensory uncertainty on the current trial. Reduced stimulus contrast was associated with an increased bias toward the stimulus direction of the previous trial. Critically, performance feedback, which reduced sensory uncertainty, abolished serial dependence. These results provide clear evidence for a post-perceptual locus of serial dependence in 3D motion perception and support the role of serial dependence as a response strategy in the face of substantial sensory uncertainty.

Asymmetries in the discrimination of motion direction around the visual field.

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.

Perspective Cues Make Eye-specific Contributions to 3-D Motion Perception.

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.

Head jitter enhances three-dimensional motion perception.

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.

Contributions of binocular and monocular cues to motion-in-depth perception.

Intercepting and avoiding moving objects requires accurate motion-in-depth (MID) perception. Such motion can be estimated based on both binocular and monocular cues. Because previous studies largely characterized sensitivity to these cues individually, their relative contributions to MID perception remain unclear. Here we measured sensitivity to binocular, monocular, and combined cue MID stimuli using a motion coherence paradigm. We first confirmed prior reports of substantial variability in binocular MID cue sensitivity across the visual field. The stimuli were matched for eccentricity and speed, suggesting that this variability has a neural basis. Second, we determined that monocular MID cue sensitivity also varied considerably across the visual field. A major component of this variability was geometric: An MID stimulus produces the largest motion signals in the eye contralateral to its visual field location. This resulted in better monocular discrimination performance when the contralateral rather than ipsilateral eye was stimulated. Third, we found that monocular cue sensitivity generally exceeded, and was independent of, binocular cue sensitivity. Finally, contralateral monocular cue sensitivity was found to be a strong predictor of combined cue sensitivity. These results reveal distinct factors constraining the contributions of binocular and monocular cues to three-dimensional motion perception.

Systematic misperceptions of 3-D motion explained by Bayesian inference.

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.

Inhibition of Lateral Prefrontal Cortex Produces Emotionally Biased First Impressions: A Transcranial Magnetic Stimulation and Electroencephalography Study.

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.

Impaired Velocity Processing Reveals an Agnosia for Motion in Depth.

Many individuals with normal visual acuity are unable to discriminate the direction of 3-D motion in a portion of their visual field, a deficit previously referred to as a stereomotion scotoma. The origin of this visual deficit has remained unclear. We hypothesized that the impairment is due to a failure in the processing of one of the two binocular cues to motion in depth: changes in binocular disparity over time or interocular velocity differences. We isolated the contributions of these two cues and found that sensitivity to interocular velocity differences, but not changes in binocular disparity, varied systematically with observers' ability to judge motion direction. We therefore conclude that the inability to interpret motion in depth is due to a failure in the neural mechanisms that combine velocity signals from the two eyes. Given these results, we argue that the deficit should be considered a prevalent but previously unrecognized agnosia specific to the perception of visual motion.

Sensitivity and bias in the discrimination of two-dimensional and three-dimensional motion direction.

Sensory systems are faced with an essentially infinite number of possible environmental events but have limited processing resources. Posed with this challenge, it makes sense to allocate these resources to prioritize the discrimination of events with the most behavioral relevance. Here, we asked if such relevance is reflected in the processing and perception of motion. We compared human performance on a rapid motion direction discrimination task, including monocular and binocular viewing. In particular, we determined sensitivity and bias for a binocular motion-in-depth (three-dimensional; 3D) stimulus and for its constituent monocular (two-dimensional; 2D) signals over a broad range of speeds. Consistent with prior work, we found that binocular 3D sensitivity was lower than monocular sensitivity for all speeds. Although overall sensitivity was worse for 3D discrimination, we found that the transformation from 2D to 3D motion processing also incorporated a pattern of potentially advantageous biases. One such bias is reflected by a criterion shift that occurs at the level of 3D motion processing and results in an increased hit rate for motion toward the head. We also observed an increase in sensitivity for 3D motion trajectories presented on crossed rather than uncrossed disparity pedestals, privileging motion trajectories closer to the observer. We used these measurements to determine the range of real-world trajectories for which rapid 3D motion discrimination is most useful. These results suggest that the neural mechanisms that underlie motion perception privilege behaviorally relevant motion and provide insights into the nature of human motion sensitivity in the real world.

Nonconscious emotional activation colors first impressions: a regulatory role for conscious awareness.

Emotions can color people's attitudes toward unrelated objects in the environment. Existing evidence suggests that such emotional coloring is particularly strong when emotion-triggering information escapes conscious awareness. But is emotional reactivity stronger after nonconscious emotional provocation than after conscious emotional provocation, or does conscious processing specifically change the association between emotional reactivity and evaluations of unrelated objects? In this study, we independently indexed emotional reactivity and coloring as a function of emotional-stimulus awareness to disentangle these accounts. Specifically, we recorded skin-conductance responses to spiders and fearful faces, along with subsequent preferences for novel neutral faces during visually aware and unaware states. Fearful faces increased skin-conductance responses comparably in both stimulus-aware and stimulus-unaware conditions. Yet only when visual awareness was precluded did skin-conductance responses to fearful faces predict decreased likability of neutral faces. These findings suggest a regulatory role for conscious awareness in breaking otherwise automatic associations between physiological reactivity and evaluative emotional responses.

Contour extracting networks in early extrastriate cortex.

Neurons in the visual cortex process a local region of visual space, but in order to adequately analyze natural images, neurons need to interact. The notion of an ''association field'' proposes that neurons interact to extract extended contours. Here, we identify the site and properties of contour integration mechanisms. We used functional magnetic resonance imaging (fMRI) and population receptive field (pRF) analyses. We devised pRF mapping stimuli consisting of contours. We isolated the contribution of contour integration mechanisms to the pRF by manipulating the contour content. This stimulus manipulation led to systematic changes in pRF size. Whereas a bank of Gabor filters quantitatively explains pRF size changes in V1, only V2/V3 pRF sizes match the predictions of the association field. pRF size changes in later visual field maps, hV4, LO-1, and LO-2 do not follow either prediction and are probably driven by distinct classical receptive field properties or other extraclassical integration mechanisms. These pRF changes do not follow conventional fMRI signal strength measures. Therefore, analyses of pRF changes provide a novel computational neuroimaging approach to investigating neural interactions. We interpreted these results as evidence for neural interactions along cooriented, cocircular receptive fields in the early extrastriate visual cortex (V2/V3), consistent with the notion of a contour association field.

Tracts in the limbic system show microstructural alterations post COVID-19 recovery.

Delirium, memory loss, attention deficit and fatigue are frequently reported by COVID survivors, yet the neurological pathways underlying these symptoms are not well understood. To study the possible mechanisms for these long-term sequelae after COVID-19 recovery, we investigated the microstructural properties of white matter in Indian cohorts of COVID-recovered patients and healthy controls. For the cross-sectional study presented here, we recruited 44 COVID-recovered patients and 29 healthy controls in New Delhi, India. Using deterministic whole-brain tractography on the acquired diffusion MRI scans, we traced 20 white matter tracts and compared fractional anisotropy, axial, mean and radial diffusivity between the cohorts. Our results revealed statistically significant differences (PFWE < 0.01) in the uncinate fasciculus, cingulum cingulate, cingulum hippocampus and arcuate fasciculus in COVID survivors, suggesting the presence of microstructural abnormalities. Additionally, in a subsequent subgroup analysis based on infection severity (healthy control, non-hospitalized patients and hospitalized patients), we observed a correlation between tract diffusion measures and COVID-19 infection severity. Although there were significant differences between healthy controls and infected groups, we found no significant differences between hospitalized and non-hospitalized COVID patients. Notably, the identified tracts are part of the limbic system and orbitofrontal cortex, indicating microstructural differences in neural circuits associated with memory and emotion. The observed white matter alterations in the limbic system resonate strongly with the functional deficits reported in Long COVID. Overall, our study provides additional evidence that damage to the limbic system could be a neuroimaging signature of Long COVID. The findings identify targets for follow-up studies investigating the long-term physiological and psychological impact of COVID-19.

Hierarchical computation of 3D motion across macaque areas MT and FST.

Computing behaviorally relevant representations of three-dimensional (3D) motion from two-dimensional (2D) retinal signals is critical for survival. To ascertain where and how the primate visual system performs this computation, we recorded from the macaque middle temporal (MT) area and its downstream target, the fundus of the superior temporal sulcus (area FST). Area MT is a key site of 2D motion processing, but its role in 3D motion processing is controversial. The functions of FST remain highly underexplored. To distinguish representations of 3D motion from those of 2D retinal motion, we contrast responses to multiple motion cues during a motion discrimination task. The results reveal a hierarchical transformation whereby many FST but not MT neurons are selective for 3D motion. Modeling results further show how generalized, cue-invariant representations of 3D motion in FST may be created by selectively integrating the output of 2D motion selective MT neurons.

A General Framework for Inferring Bayesian Ideal Observer Models from Psychophysical Data.

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.

To CD or not to CD: Is there a 3D motion aftereffect based on changing disparities?

Recently, T. B. Czuba, B. Rokers, K. Guillet, A. C. Huk, and L. K. Cormack, (2011) and Y. Sakano, R. S. Allison, and I. P. Howard (2012) published very similar studies using the motion aftereffect to probe the way in which motion through depth is computed. Here, we compare and contrast the findings of these two studies and incorporate their results with a brief follow-up experiment. Taken together, the results leave no doubt that the human visual system incorporates a mechanism that is uniquely sensitive to the difference in velocity signals between the two eyes, but--perhaps surprisingly--evidence for a neural representation of changes in binocular disparity over time remains elusive.

Motion processing with two eyes in three dimensions.

The movement of an object toward or away from the head is perhaps the most critical piece of information an organism can extract from its environment. Such 3D motion produces horizontally opposite motions on the two retinae. Little is known about how or where the visual system combines these two retinal motion signals, relative to the wealth of knowledge about the neural hierarchies involved in 2D motion processing and binocular vision. Canonical conceptions of primate visual processing assert that neurons early in the visual system combine monocular inputs into a single cyclopean stream (lacking eye-of-origin information) and extract 1D ("component") motions; later stages then extract 2D pattern motion from the cyclopean output of the earlier stage. Here, however, we show that 3D motion perception is in fact affected by the comparison of opposite 2D pattern motions between the two eyes. Three-dimensional motion sensitivity depends systematically on pattern motion direction when dichoptically viewing gratings and plaids-and a novel "dichoptic pseudoplaid" stimulus provides strong support for use of interocular pattern motion differences by precluding potential contributions from conventional disparity-based mechanisms. These results imply the existence of eye-of-origin information in later stages of motion processing and therefore motivate the incorporation of such eye-specific pattern-motion signals in models of motion processing and binocular integration.

Three-dimensional motion aftereffects reveal distinct direction-selective mechanisms for binocular processing of motion through depth.

Motion aftereffects are historically considered evidence for neuronal populations tuned to specific directions of motion. Despite a wealth of motion aftereffect studies investigating 2D (frontoparallel) motion mechanisms, there is a remarkable dearth of psychophysical evidence for neuronal populations selective for the direction of motion through depth (i.e., tuned to 3D motion). We compared the effects of prolonged viewing of unidirectional motion under dichoptic and monocular conditions and found large 3D motion aftereffects that could not be explained by simple inheritance of 2D monocular aftereffects. These results (1) demonstrate the existence of neurons tuned to 3D motion as distinct from monocular 2D mechanisms, (2) show that distinct 3D direction selectivity arises from both interocular velocity differences and changing disparities over time, and (3) provide a straightforward psychophysical tool for further probing 3D motion mechanisms.

Speed and eccentricity tuning reveal a central role for the velocity-based cue to 3D visual motion.

Two binocular cues are thought to underlie the visual perception of three-dimensional (3D) motion: a disparity-based cue, which relies on changes in disparity over time, and a velocity-based cue, which relies on interocular velocity differences. The respective building blocks of these cues, instantaneous disparity and retinal motion, exhibit very distinct spatial and temporal signatures. Although these two cues are synchronous in naturally moving objects, disparity-based and velocity-based mechanisms can be dissociated experimentally. We therefore investigated how the relative contributions of these two cues change across a range of viewing conditions. We measured direction-discrimination sensitivity for motion though depth across a wide range of eccentricities and speeds for disparity-based stimuli, velocity-based stimuli, and "full cue" stimuli containing both changing disparities and interocular velocity differences. Surprisingly, the pattern of sensitivity for velocity-based stimuli was nearly identical to that for full cue stimuli across the entire extent of the measured spatiotemporal surface and both were clearly distinct from those for the disparity-based stimuli. These results suggest that for direction discrimination outside the fovea, 3D motion perception primarily relies on the velocity-based cue with little, if any, contribution from the disparity-based cue.