Continuous psychophysics shows millisecond-scale visual processing delays are faithfully preserved in movement dynamics.

Image differences between the eyes can cause interocular discrepancies in the speed of visual processing. Millisecond-scale differences in visual processing speed can cause dramatic misperceptions of the depth and three-dimensional direction of moving objects. Here, we develop a monocular and binocular continuous target-tracking psychophysics paradigm that can quantify such tiny differences in visual processing speed. Human observers continuously tracked a target undergoing Brownian motion with a range of luminance levels in each eye. Suitable analyses recover the time course of the visuomotor response in each condition, the dependence of visual processing speed on luminance level, and the temporal evolution of processing differences between the eyes. Importantly, using a direct within-observer comparison, we show that continuous target-tracking and traditional forced-choice psychophysical methods provide estimates of interocular delays that agree on average to within a fraction of a millisecond. Thus, visual processing delays are preserved in the movement dynamics of the hand. Finally, we show analytically, and partially confirm experimentally, that differences between the temporal impulse response functions in the two eyes predict how lateral target motion causes misperceptions of motion in depth and associated tracking responses. Because continuous target tracking can accurately recover millisecond-scale differences in visual processing speed and has multiple advantages over traditional psychophysics, it should facilitate the study of temporal processing in the future.

Retinal motion statistics during natural locomotion.

Walking through an environment generates retinal motion, which humans rely on to perform a variety of visual tasks. Retinal motion patterns are determined by an interconnected set of factors, including gaze location, gaze stabilization, the structure of the environment, and the walker's goals. The characteristics of these motion signals have important consequences for neural organization and behavior. However, to date, there are no empirical in situ measurements of how combined eye and body movements interact with real 3D environments to shape the statistics of retinal motion signals. Here, we collect measurements of the eyes, the body, and the 3D environment during locomotion. We describe properties of the resulting retinal motion patterns. We explain how these patterns are shaped by gaze location in the world, as well as by behavior, and how they may provide a template for the way motion sensitivity and receptive field properties vary across the visual field.

Stereo slant discrimination of planar 3D surfaces: Frontoparallel versus planar matching.

Binocular stereo cues are important for discriminating 3D surface orientation, especially at near distances. We devised a single-interval task where observers discriminated the slant of a densely textured planar test surface relative to a textured planar surround reference surface. Although surfaces were rendered with correct perspective, the stimuli were designed so that the binocular cues dominated performance. Slant discrimination performance was measured as a function of the reference slant and the level of uncorrelated white noise added to the test-plane images in the left and right eyes. We compared human performance with an approximate ideal observer (planar matching [PM]) and two subideal observers. The PM observer uses the image in one eye and back projection to predict a test image in the other eye for all possible slants, tilts, and distances. The estimated slant, tilt, and distance are determined by the prediction that most closely matches the measured image in the other eye. The first subideal observer (local planar matching [LPM]) applies PM over local neighborhoods and then pools estimates across the test plane. The second suboptimal observer (local frontoparallel matching [LFM]) uses only location disparity. We find that the ideal observer (PM) and the first subideal observer (LPM) outperforms the second subideal observer (LFM), demonstrating the additional benefit of pattern disparities. We also find that all three model observers can account for human performance, if two free parameters are included: a fixed small level of internal estimation noise, and a fixed overall efficiency scalar on slant discriminability.

Recent understanding of binocular vision in the natural environment with clinical implications.

Technological advances in recent decades have allowed us to measure both the information available to the visual system in the natural environment and the rich array of behaviors that the visual system supports. This review highlights the tasks undertaken by the binocular visual system in particular and how, for much of human activity, these tasks differ from those considered when an observer fixates a static target on the midline. The everyday motor and perceptual challenges involved in generating a stable, useful binocular percept of the environment are discussed, together with how these challenges are but minimally addressed by much of current clinical interpretation of binocular function. The implications for new technology, such as virtual reality, are also highlighted in terms of clinical and basic research application.

Effects of endocrine-disrupting chemicals on hypothalamic oxytocin and vasopressin systems.

Exposures to endocrine disrupting chemicals (EDCs) perturb hormonal systems. EDCs are particularly problematic when exposure happens in the fetus and infant due to the high sensitivity of developing organisms to hormone actions. Previous work has shown that prenatal polychlorinated biphenyl (PCB) exposure disrupts hypothalamic development, reproductive physiology, mate preference behavior, and social behaviors in a sexually dimorphic manner. Based on evidence that EDCs perturb social behaviors in rodents, we examined effects of PCBs on the neuropeptides oxytocin (OXT) and vasopressin (AVP) that are involved in regulating these behaviors. Rats were exposed prenatally (gestational days 16 and 18) to the weakly estrogenic PCB mixture Aroclor 1221 (0.5 or 1 mg/kg), to estradiol benzoate (EB, a positive control), or to the vehicle (3% dimethyl sulfoxide). In adult (~P90) brains, we counted immunolabeled oxytocin and vasopressin cell numbers in the paraventricular nucleus (PVN) and supraoptic nucleus (SON) of the hypothalamus. EDCs did not change absolute numbers of oxytocin or vasopressin cells in either region, although there were some modest shifts in the rostral-caudal distribution. Second, expression of genes for these nonapeptides (Oxt, Avp), their receptors (Oxtr, Avpr1a), and the estrogen receptor beta (Esr2), was determined by qPCR. In the PVN, there were dose-dependent effects of PCBs in males (Oxt, Oxtr), and effects of EB in females (Avp, Esr2). In the SON, Oxt, and Esr2 were affected by treatments in males. These changes to protein and gene expression caused by prenatal treatments suggest that transcriptional and posttranscriptional mechanisms play roles in mediating how EDCs reprogram hypothalamic development.

Spatiotemporal integration of isolated binocular three-dimensional motion cues.

Two primary binocular cues-based on velocities seen by the two eyes or on temporal changes in binocular disparity-support the perception of three-dimensional (3D) motion. Although these cues support 3D motion perception in different perceptual tasks or regimes, stimulus cross-cue contamination and/or substantial differences in spatiotemporal structure have complicated interpretations. We introduce novel psychophysical stimuli which cleanly isolate the cues, based on a design introduced in oculomotor work (Sheliga, Quaia, FitzGibbon, & Cumming, 2016). We then use these stimuli to characterize and compare the temporal and spatial integration properties of velocity- and disparity-based mechanisms. On average, temporal integration of velocity-based cues progressed more than twice as quickly as disparity-based cues; performance in each pure-cue condition saturated at approximately 200 ms and approximately 500 ms, respectively. This temporal distinction suggests that disparity-based 3D direction judgments may include a post-sensory stage involving additional integration time in some observers, whereas velocity-based judgments are rapid and seem to be more purely sensory in nature. Thus, these two binocular mechanisms appear to support 3D motion perception with distinct temporal properties, reflecting differential mixtures of sensory and decision contributions. Spatial integration profiles for the two mechanisms were similar, and on the scale of receptive fields in area MT. Consistent with prior work, there were substantial individual differences, which we interpret as both sensory and cognitive variations across subjects, further clarifying the case for distinct sets of both cue-specific sensory and cognitive mechanisms. The pure-cue stimuli presented here lay the groundwork for further investigations of velocity- and disparity-based contributions to 3D motion perception.

Binocular viewing geometry shapes the neural representation of the dynamic three-dimensional environment.

Sensory signals give rise to patterns of neural activity, which the brain uses to infer properties of the environment. For the visual system, considerable work has focused on the representation of frontoparallel stimulus features and binocular disparities. However, inferring the properties of the physical environment from retinal stimulation is a distinct and more challenging computational problem-this is what the brain must actually accomplish to support perception and action. Here we develop a computational model that incorporates projective geometry, mapping the three-dimensional (3D) environment onto the two retinae. We demonstrate that this mapping fundamentally shapes the tuning of cortical neurons and corresponding aspects of perception. For 3D motion, the model explains the strikingly non-canonical tuning present in existing electrophysiological data and distinctive patterns of perceptual errors evident in human behavior. Decoding the world from cortical activity is strongly affected by the geometry that links the environment to the sensory epithelium.

Eye-specific pattern-motion signals support the perception of three-dimensional motion.

An object moving through three-dimensional (3D) space typically yields different patterns of velocities in each eye. For an interocular velocity difference cue to be used, some instances of real 3D motion in the environment (e.g., when a moving object is partially occluded) would require an interocular velocity difference computation that operates on motion signals that are not only monocular (or eye specific) but also depend on each eye's two-dimensional (2D) direction being estimated over regions larger than the size of V1 receptive fields (i.e., global pattern motion). We investigated this possibility using 3D motion aftereffects (MAEs) with stimuli comprising many small, drifting Gabor elements. Conventional frontoparallel (2D) MAEs were local-highly sensitive to the test elements being in the same locations as the adaptor (Experiment 1). In contrast, 3D MAEs were robust to the test elements being in different retinal locations than the adaptor, indicating that 3D motion processing involves relatively global spatial pooling of motion signals (Experiment 2). The 3D MAEs were strong even when the local elements were in unmatched locations across the two eyes during adaptation, as well as when the adapting stimulus elements were randomly oriented, and specified global motion via the intersection of constraints (Experiment 3). These results bolster the notion of eye-specific computation of 2D pattern motion (involving global pooling of local, eye-specific motion signals) for the purpose of computing 3D motion, and highlight the idea that classically "late" computations such as pattern motion can be done in a manner that retains information about the eye of origin.

Daily consumption of methylene blue reduces attentional deficits and dopamine reduction in a 6-OHDA model of Parkinson's disease.

Recently, alternative drug therapies for Parkinson's disease (PD) have been investigated as there are many shortcomings of traditional dopamine-based therapies including difficulties in treating cognitive and attentional dysfunction. A promising therapeutic avenue is to target mitochondrial dysfunction and oxidative stress in PD. One option might be the use of methylene blue (MB), an antioxidant and metabolic enhancer. MB has been shown to improve cognitive function in both intact rodents and rodent disease models. Therefore, we investigated whether MB might treat attentional deficits in a rat model of PD induced by 6-hydroxydopamine (6-OHDA). MB also has neuroprotective capabilities against neurotoxic insult, so we also assessed the ability of MB to provide neuroprotection in our PD model. The results show that MB could preserve some dopamine neurons in the substantia nigra par compacta when 6-OHDA was infused into the medial forebrain bundle. This neuroprotection did not yield a significant behavioral improvement when motor functions were measured. However, MB significantly improved attentional performance in the five-choice task designed to measure selective and sustained attention. In conclusion, MB might be useful in improving some attentional function and preserving dopaminergic cells in this model. Future work should continue to study and optimize the abilities of MB for the treatment of PD.

Binocular Mechanisms of 3D Motion Processing.

The visual system must recover important properties of the external environment if its host is to survive. Because the retinae are effectively two-dimensional but the world is three-dimensional (3D), the patterns of stimulation both within and across the eyes must be used to infer the distal stimulus-the environment-in all three dimensions. Moreover, animals and elements in the environment move, which means the input contains rich temporal information. Here, in addition to reviewing the literature, we discuss how and why prior work has focused on purported isolated systems (e.g., stereopsis) or cues (e.g., horizontal disparity) that do not necessarily map elegantly on to the computations and complex patterns of stimulation that arise when visual systems operate within the real world. We thus also introduce the binoptic flow field (BFF) as a description of the 3D motion information available in realistic environments, which can foster the use of ecologically valid yet well-controlled stimuli. Further, it can help clarify how future studies can more directly focus on the computations and stimulus properties the visual system might use to support perception and behavior in a dynamic 3D world.

Bayesian depth estimation from monocular natural images.

Estimating an accurate and naturalistic dense depth map from a single monocular photographic image is a difficult problem. Nevertheless, human observers have little difficulty understanding the depth structure implied by photographs. Two-dimensional (2D) images of the real-world environment contain significant statistical information regarding the three-dimensional (3D) structure of the world that the vision system likely exploits to compute perceived depth, monocularly as well as binocularly. Toward understanding how this might be accomplished, we propose a Bayesian model of monocular depth computation that recovers detailed 3D scene structures by extracting reliable, robust, depth-sensitive statistical features from single natural images. These features are derived using well-accepted univariate natural scene statistics (NSS) models and recent bivariate/correlation NSS models that describe the relationships between 2D photographic images and their associated depth maps. This is accomplished by building a dictionary of canonical local depth patterns from which NSS features are extracted as prior information. The dictionary is used to create a multivariate Gaussian mixture (MGM) likelihood model that associates local image features with depth patterns. A simple Bayesian predictor is then used to form spatial depth estimates. The depth results produced by the model, despite its simplicity, correlate well with ground-truth depths measured by a current-generation terrestrial light detection and ranging (LIDAR) scanner. Such a strong form of statistical depth information could be used by the visual system when creating overall estimated depth maps incorporating stereopsis, accommodation, and other conditions. Indeed, even in isolation, the Bayesian predictor delivers depth estimates that are competitive with state-of-the-art "computer vision" methods that utilize highly engineered image features and sophisticated machine learning algorithms.

Dynamic mechanisms of visually guided 3D motion tracking.

The continuous perception of motion-through-depth is critical for both navigation and interacting with objects in a dynamic three-dimensional (3D) world. Here we used 3D tracking to simultaneously assess the perception of motion in all directions, facilitating comparisons of responses to motion-through-depth to frontoparallel motion. Observers manually tracked a stereoscopic target as it moved in a 3D Brownian random walk. We found that continuous tracking of motion-through-depth was selectively impaired, showing different spatiotemporal properties compared with frontoparallel motion tracking. Two separate factors were found to contribute to this selective impairment. The first is the geometric constraint that motion-through-depth yields much smaller retinal projections than frontoparallel motion, given the same object speed in the 3D environment. The second factor is the sluggish nature of disparity processing, which is present even for frontoparallel motion tracking of a disparity-defined stimulus. Thus, despite the ecological importance of reacting to approaching objects, both the geometry of 3D vision and the nature of disparity processing result in considerable impairments for tracking motion-through-depth using binocular cues.NEW & NOTEWORTHY We characterize motion perception continuously in all directions using an ecologically relevant, manual target tracking paradigm we recently developed. This approach reveals a selective impairment to the perception of motion-through-depth. Geometric considerations demonstrate that this impairment is not consistent with previously observed spatial deficits (e.g., stereomotion suppression). However, results from an examination of disparity processing are consistent with the longer latencies observed in discrete, trial-based measurements of the perception of motion-through-depth.

Reconsolidation-Extinction Interactions in Fear Memory Attenuation: The Role of Inter-Trial Interval Variability.

Fear extinction typically results in the formation of a new inhibitory memory that suppresses the original conditioned response. Evidence also suggests that extinction training during a retrieval-induced labile period results in integration of the extinction memory into the original fear memory, rendering the fear memory less susceptible to reinstatement. Here we investigated the parameters by which the retrieval-extinction paradigm was most effective in memory updating. Specifically, we manipulated the inter-trial intervals (ITIs) between conditional stimulus (CS) presentations during extinction, examining how having interval lengths with different degrees of variability affected the strength of memory updating. We showed that randomizing the ITI of CS presentations during extinction led to less return of fear via reinstatement than extinction with a fixed ITI. Subjects who received variable ITIs during extinction also showed higher freezing during the ITI, indicating that the randomization of CS presentations led to a higher general reactivity during extinction, which may be one potential mechanism for memory updating.

Negative Affect-Associated USV Acoustic Characteristics Predict Future Excessive Alcohol Drinking and Alcohol Avoidance in Male P and NP Rats.

BACKGROUND: Negative emotional status and adverse emotional events increase vulnerability to alcohol abuse. Ultrasonic vocalizations (USVs) emitted by rats are a well-established model of emotional status that can reflect positive or negative affective responses in real time. Most USV studies assess counts, yet each USV is a multidimensional data point characterized by several acoustic characteristics that may provide insight into the neurocircuitry underlying emotional response. METHODS: USVs emitted from selectively bred alcohol-naïve and alcohol-experienced alcohol-preferring and nonpreferring rats (P and NP rats) were recorded during 4-hour sessions on alternating days over 4 weeks. Linear mixed modeling (LMM) and linear discriminant analysis (LDA) were applied to USV acoustic characteristics (e.g., frequency, duration, power, and bandwidth) of negative affect (22 to 28 kilohertz [kHz])- and positive (50 to 55 kHz) affect-related USVs. RESULTS: Hundred percent separation between alcohol-naïve P and NP rats was achieved through a linear combination (produced by LDA) of USV acoustic characteristics of 22- to 28-kHz USVs, whereas poor separation (36.5%) was observed for 50- to 55-kHz USVs. 22- to 28-kHz LDA separation was high (87%) between alcohol-experienced P and NP rats, but was poor for 50- to 55-kHz USVs (57.3%). USV mean frequency and duration were the highest weighted characteristics in both the naïve and experienced 22- to 28-kHz LDA representations suggesting that alcohol experience does not alter the representations. LMM analyses of 22- to 28-kHz USV acoustic characteristics matched the LDA results. Poor LDA separation was observed between alcohol-naïve and alcohol-experienced P rats for both 22- to 28-kHz and 50- to 55-kHz USVs. CONCLUSIONS: Advanced statistical analysis of negative affect-associated USV data predicts future behaviors of excessive alcohol drinking and alcohol avoidance in selectively bred rats. USV characteristics across rat lines reveal affect-related motivation to consume alcohol and may predict neural pathways mediating emotional response. Further characterization of these differences could delineate particular neurocircuitry and methods to ameliorate dysregulated emotional states often observed in human alcohol abusers.

Separate Perceptual and Neural Processing of Velocity- and Disparity-Based 3D Motion Signals.

Although the visual system uses both velocity- and disparity-based binocular information for computing 3D motion, it is unknown whether (and how) these two signals interact. We found that these two binocular signals are processed distinctly at the levels of both cortical activity in human MT and perception. In human MT, adaptation to both velocity-based and disparity-based 3D motions demonstrated direction-selective neuroimaging responses. However, when adaptation to one cue was probed using the other cue, there was no evidence of interaction between them (i.e., there was no "cross-cue" adaptation). Analogous psychophysical measurements yielded correspondingly weak cross-cue motion aftereffects (MAEs) in the face of very strong within-cue adaptation. In a direct test of perceptual independence, adapting to opposite 3D directions generated by different binocular cues resulted in simultaneous, superimposed, opposite-direction MAEs. These findings suggest that velocity- and disparity-based 3D motion signals may both flow through area MT but constitute distinct signals and pathways. SIGNIFICANCE STATEMENT: Recent human neuroimaging and monkey electrophysiology have revealed 3D motion selectivity in area MT, which is driven by both velocity-based and disparity-based 3D motion signals. However, to elucidate the neural mechanisms by which the brain extracts 3D motion given these binocular signals, it is essential to understand how-or indeed if-these two binocular cues interact. We show that velocity-based and disparity-based signals are mostly separate at the levels of both fMRI responses in area MT and perception. Our findings suggest that the two binocular cues for 3D motion might be processed by separate specialized mechanisms.

Speed discrimination in the far monocular periphery: A relative advantage for interocular comparisons consistent with self-motion.

Some animals with lateral eyes (such as bees) control their navigation through the 3D world using velocity differences between the two eyes. Other animals with frontal eyes (such as primates, including humans) can perceive 3D motion based on the different velocities that a moving object projects upon the two retinae. Although one type of 3D motion perception involves a comparison between velocities from vastly different (monocular) portions of the visual field, and the other involves a comparison within overlapping (binocular) portions of the visual field, both compare velocities across the two eyes. Here we asked whether human interocular velocity comparisons, typically studied in the context of binocularly overlapping vision, operate in the far lateral (and hence, monocular) periphery and, if so, whether these comparisons were accordant with conventional interocular motion processing. We found that speed discrimination was indeed better between the two eyes' monocular visual fields, as compared to within a single eye's (monocular) visual field, but only when the velocities were consistent with commonly encountered motion. This intriguing finding suggests that mechanisms sensitive to relative motion information on opposite sides of an animal may have been retained, or at some point independently achieved, as the eyes became frontal in some animals.

The effect of eccentricity and spatiotemporal energy on motion silencing.

The now well-known motion-silencing illusion has shown that salient changes among a group of objects' luminances, colors, shapes, or sizes may appear to cease when objects move rapidly (Suchow & Alvarez, 2011). It has been proposed that silencing derives from dot spacing that causes crowding, coherent changes in object color or size, and flicker frequencies combined with dot spacing (Choi, Bovik, & Cormack, 2014; Peirce, 2013; Turi & Burr, 2013). Motion silencing is a peripheral effect that does not occur near the point of fixation. To better understand the effect of eccentricity on motion silencing, we measured the amount of motion silencing as a function of eccentricity in human observers using traditional psychophysics. Fifteen observers reported whether dots in any of four concentric rings changed in luminance over a series of rotational velocities. The results in the human experiments showed that the threshold velocity for motion silencing almost linearly decreases as a function of log eccentricity. Further, we modeled the response of a population of simulated V1 neurons to our stimuli. We found strong matches between the threshold velocities on motion silencing observed in the human experiment and those seen in the energy model of Adelson and Bergen (1985). We suggest the plausible explanation that as eccentricity increases, the combined motion-flicker signal falls outside the narrow spatiotemporal frequency response regions of the modeled receptive fields, thereby reducing flicker visibility.

A Distinct Mechanism of Temporal Integration for Motion through Depth.

Temporal integration of visual motion has been studied extensively within the frontoparallel plane (i.e., 2D). However, the majority of motion occurs within a 3D environment, and it is unknown whether the principles from 2D motion processing generalize to more realistic 3D motion. We therefore characterized and compared temporal integration underlying 2D (left/right) and 3D (toward/away) direction discrimination in human observers, varying motion coherence across a range of viewing durations. The resulting discrimination-versus-duration functions followed three stages, as follows: (1) a steep improvement during the first ∼150 ms, likely reflecting early sensory processing; (2) a subsequent, more gradual benefit of increasing duration over several hundreds of milliseconds, consistent with some form of temporal integration underlying decision formation; and (3) a final stage in which performance ceased to improve with duration over ∼1 s, which is consistent with an upper limit on integration. As previously found, improvements in 2D direction discrimination with time were consistent with near-perfect integration. In contrast, 3D motion sensitivity was lower overall and exhibited a substantial departure from perfect integration. These results confirm that there are overall differences in sensitivity for 2D and 3D motion that are consistent with a sensory difference between binocular and dichoptic sensory mechanisms. They also reveal a difference at the integration stage, in which 3D motion is not accumulated as perfectly as in the 2D motion model system.

Continuous psychophysics: Target-tracking to measure visual sensitivity.

We introduce a novel framework for estimating visual sensitivity using a continuous target-tracking task in concert with a dynamic internal model of human visual performance. Observers used a mouse cursor to track the center of a two-dimensional Gaussian luminance blob as it moved in a random walk in a field of dynamic additive Gaussian luminance noise. To estimate visual sensitivity, we fit a Kalman filter model to the human tracking data under the assumption that humans behave as Bayesian ideal observers. Such observers optimally combine prior information with noisy observations to produce an estimate of target position at each time step. We found that estimates of human sensory noise obtained from the Kalman filter fit were highly correlated with traditional psychophysical measures of human sensitivity (R2 > 97%). Because each frame of the tracking task is effectively a "minitrial," this technique reduces the amount of time required to assess sensitivity compared with traditional psychophysics. Furthermore, because the task is fast, easy, and fun, it could be used to assess children, certain clinical patients, and other populations that may get impatient with traditional psychophysics. Importantly, the modeling framework provides estimates of decision variable variance that are directly comparable with those obtained from traditional psychophysics. Further, we show that easily computed summary statistics of the tracking data can also accurately predict relative sensitivity (i.e., traditional sensitivity to within a scale factor).