Testing Neuronal Accounts of Anisotropic Motion Perception with Computational Modelling

There is an over-representation of neurons in early visual cortical areas that respond most strongly to cardinal (horizontal and vertical) orientations and directions of visual stimuli, and cardinal- and oblique-preferring neurons are reported to have different tuning curves. Collectively, these neuronal anisotropies can explain two commonly-reported phenomena of motion perception – the oblique effect and reference repulsion – but it remains unclear whether neuronal anisotropies can simultaneously account for both perceptual effects. We show in psychophysical experiments that reference repulsion and the oblique effect do not depend on the duration of a moving stimulus, and that brief adaptation to a single direction simultaneously causes a reference repulsion in the orientation domain, and the inverse of the oblique effect in the direction domain. We attempted to link these results to underlying neuronal anisotropies by implementing a large family of neuronal decoding models with parametrically varied levels of anisotropy in neuronal direction-tuning preferences, tuning bandwidths and spiking rates. Surprisingly, no model instantiation was able to satisfactorily explain our perceptual data. We argue that the oblique effect arises from the anisotropic distribution of preferred directions evident in V1 and MT, but that reference repulsion occurs separately, perhaps reflecting a process of categorisation occurring in higher-order cortical areas.     

Using Low Levels of Stochastic Vestibular Stimulation to Improve Balance Function

Low-level stochastic vestibular stimulation (SVS) has been associated with improved postural responses in the medio-lateral (ML) direction, but its effect in improving balance function in both the ML and anterior-posterior (AP) directions has not been studied. In this series of studies, the efficacy of applying low amplitude SVS in 0–30 Hz range between the mastoids in the ML direction on improving cross-planar balance function was investigated. Forty-five (45) subjects stood on a compliant surface with their eyes closed and were instructed to maintain a stable upright stance. Measures of stability of the head, trunk, and whole body were quantified in ML, AP and combined APML directions. Results show that binaural bipolar SVS given in the ML direction significantly improved balance performance with the peak of optimal stimulus amplitude predominantly in the range of 100–500 μA for all the three directions, exhibiting stochastic resonance (SR) phenomenon. Objective perceptual and body motion thresholds as estimates of internal noise while subjects sat on a chair with their eyes closed and were given 1 Hz bipolar binaural sinusoidal electrical stimuli were also measured. In general, there was no significant difference between estimates of perceptual and body motion thresholds. The average optimal SVS amplitude that improved balance performance (peak SVS amplitude normalized to perceptual threshold) was estimated to be 46% in ML, 53% in AP, and 50% in APML directions. A miniature patch-type SVS device may be useful to improve balance function in people with disabilities due to aging, Parkinson’s disease or in astronauts returning from long-duration space flight.     

Neural correlates of contrast detection at threshold

Human psychophysical studies have demonstrated that, for stimuli near the threshold of visibility, detection of motion in one direction is unaffected by the superimposition of motion in the opposite direction. To investigate the neural basis for this perceptual phenomenon, we recorded from directionally selective neurons in macaque visual area MT (middle temporal visual area). Contrast thresholds obtained for single gratings moving in a neuron's preferred direction were compared with those obtained for motion presented simultaneously in the neuron's preferred and antipreferred directions. A simple model based on probability summation between neurons tuned to opposite directions could sufficiently account for contrast thresholds revealed psychophysically, suggesting that area MT is likely to provide the neural basis for contrast detection of stimuli modulated in time.     

Directional anisotropies reveal a functional segregation of visual motion processing for perception and action

Human exhibits an anisotropy in direction perception: discrimination is superior when motion is around horizontal or vertical rather than diagonal axes. In contrast to the consistent directional anisotropy in perception, we found only small idiosyncratic anisotropies in smooth pursuit eye movements, a motor action requiring accurate discrimination of visual motion direction. Both pursuit and perceptual direction discrimination rely on signals from the middle temporal visual area (MT), yet analysis of multiple measures of MT neuronal responses in the macaque failed to provide evidence of a directional anisotropy. We conclude that MT represents different motion directions uniformly, and subsequent processing creates a directional anisotropy in pathways unique to perception. Our data support the hypothesis that, at least for visual motion, perception and action are guided by inputs from separate sensory streams. The directional anisotropy of perception appears to originate after the two streams have segregated and downstream from area MT.     

Color discrimination along the cardinal chromatic axes with VECPs as an index of function of the parvocellular pathway. Correspondence of intersubject and axis variations to psychophysics

Chromatic information is carried only by the parvocellular pathway, giving the neurophysiologist the opportunity for eliciting specific responses. Further subdivision of the parvo chromatic system in two opponent chromatic mechanisms is potentially of great interest, given that the anatomical correlate seems to reside in subclasses of parvo ganglion cells that show differences both in size and in susceptibility to disease. We separately recorded responses arising from each chromatic opponent mechanism using visual stimuli chosen to belong to one of the “cardinal” chromatic axes. A calibrated color monitor, driven by a high resolution (14 bits/gun) computer board, was used for visualization of 1 c/deg isoluminant color gratings, sinusoidally modulated in time at 4 Hz. VECPs were recorded at several color contrasts along both cardinal axes, allowing extrapolation of contrast thresholds. Psychophysical thresholds were derived in the same stimulus conditions for comparison and found to correlate very well with the electrophysiologically derived values, both as intersubject and axis differences. The S-(L+M) opponent mechanism consistently yielded higher thresholds, smaller amplitude, and higher phase lag than the L-M mechanism. This finding was largely explained by the perceptual non-uniformity of the CIE chromaticity diagram. Correcting the VECP data for the perceptual differences yielded comparable responses, supporting the view that the two mechanisms are similarly represented in the cortex. In conclusion, recording of cortical responses to color contrast stimuli belonging to the cardinal chromatic axes seems a reliable procedure and may prove to be useful in performing clinical evaluations that refine the assessment of the physiology of the visual system.     

Direct evidence for encoding of motion streaks in human visual cortex

Temporal integration in the visual system causes fast-moving objects to generate static, oriented traces (‘motion streaks’), which could be used to help judge direction of motion. While human psychophysics and single-unit studies in non-human primates are consistent with this hypothesis, direct neural evidence from the human cortex is still lacking. First, we provide psychophysical evidence that faster and slower motions are processed by distinct neural mechanisms: faster motion raised human perceptual thresholds for static orientations parallel to the direction of motion, whereas slower motion raised thresholds for orthogonal orientations. We then used functional magnetic resonance imaging to measure brain activity while human observers viewed either fast (‘streaky’) or slow random dot stimuli moving in different directions, or corresponding static-oriented stimuli. We found that local spatial patterns of brain activity in early retinotopic visual cortex reliably distinguished between static orientations. Critically, a multivariate pattern classifier trained on brain activity evoked by these static stimuli could then successfully distinguish the direction of fast (‘streaky’) but not slow motion. Thus, signals encoding static-oriented streak information are present in human early visual cortex when viewing fast motion. These experiments show that motion streaks are present in the human visual system for faster motion.     

Predicting human perceptual decisions by decoding neuronal information profiles

Perception relies on the response of populations of neurons in sensory cortex. How the response profile of a neuronal population gives rise to perception and perceptual discrimination has been conceptualized in various ways. Here we suggest that neuronal population responses represent information about our environment explicitly as Fisher information (FI), which is a local measure of the variance estimate of the sensory input. We show how this sensory information can be read out and combined to infer from the available information profile which stimulus value is perceived during a fine discrimination task. In particular, we propose that the perceived stimulus corresponds to the stimulus value that leads to the same information for each of the alternative directions, and compare the model prediction to standard models considered in the literature (population vector, maximum likelihood, maximum-a-posteriori Bayesian inference). The models are applied to human performance in a motion discrimination task that induces perceptual misjudgements of a target direction of motion by task irrelevant motion in the spatial surround of the target stimulus (motion repulsion). By using the neurophysiological insight that surround motion suppresses neuronal responses to the target motion in the center, all models predicted the pattern of perceptual misjudgements. The variation of discrimination thresholds (error on the perceived value) was also explained through the changes of the total FI content with varying surround motion directions. The proposed FI decoding scheme incorporates recent neurophysiological evidence from macaque visual cortex showing that perceptual decisions do not rely on the most active neurons, but rather on the most informative neuronal responses. We statistically compare the prediction capability of the FI decoding approach and the standard decoding models. Notably, all models reproduced the variation of the perceived stimulus values for different surrounds, but with different neuronal tuning characteristics underlying perception. Compared to the FI approach the prediction power of the standard models was based on neurons with far wider tuning width and stronger surround suppression. Our study demonstrates that perceptual misjudgements can be based on neuronal populations encoding explicitly the available sensory information, and provides testable neurophysiological predictions on neuronal tuning characteristics underlying human perceptual decisions.     

Extra-retinal adaptation of cortical motion-processing areas during pursuit eye movements

Repetitive eye movement produces a compelling motion aftereffect (MAE). One mechanism thought to contribute to the illusory movement is an extra-retinal motion signal generated after adaptation. However, extra-retinal signals are also generated during pursuit. They modulate activity within cortical motion-processing area MST, helping transform retinal motion into motion in the world during an eye movement. Given the evidence that MST plays a key role in generating MAE, it may also become indirectly adapted by prolonged pursuit. To differentiate between these two extra-retinal mechanisms we examined storage of the MAE across a period of darkness. In one condition observers were told to stare at a moving pattern, an instruction that induces a more reflexive type of eye movement. In another they were told to deliberately pursue it. We found equally long MAEs when testing immediately after adaptation but not when the test was delayed by 40 s. In the case of the reflexive eye movement the delay almost completely extinguished the MAE, whereas the illusory motion following pursuit remained intact. This suggests pursuit adapts cortical motion-processing areas whereas unintentional eye movement does not. A second experiment showed that cortical mechanisms cannot be the sole determinant of pursuit-induced MAE. Following oblique pursuit, we found MAE direction changes from oblique to vertical. Perceived MAE direction appears to be influenced by a subcortical mechanism as well, one based on the relative recovery rate of horizontal and vertical eye-movement processes recruited during oblique pursuit.     

Frame of reference transformations in motion perception during smooth pursuit eye movements

Smooth pursuit eye movements change the retinal image velocity of objects in the visual field. In order to change from a retinocentric frame of reference into a head-centric one, the visual system has to take the eye movements into account. Studies on motion perception during smooth pursuit eye movements have measured either perceived speed or perceived direction during smooth pursuit to investigate this frame of reference transformation, but never both at the same time. We devised a new velocity matching task, in which participants matched both perceived speed and direction during fixation to that during pursuit. In Experiment 1, the velocity matches were determined for a range of stimulus directions, with the head-centric stimulus speed kept constant. In Experiment 2, the retinal stimulus speed was kept approximately constant, with the same range of stimulus directions. In both experiments, the velocity matches for all directions were shifted against the pursuit direction, suggesting an incomplete transformation of the frame of reference. The degree of compensation was approximately constant across stimulus direction. We fitted the classical linear model, the model of Turano and Massof (2001) and that of Freeman (2001) to the velocity matches. The model of Turano and Massof fitted the velocity matches best, but the differences between de model fits were quite small. Evaluation of the models and comparison to a few alternatives suggests that further specification of the potential effect of retinal image characteristics on the eye movement signal is needed.     

Eye gaze is not coded by cardinal mechanisms alone

Gaze is an important social cue in regulating human and non-human interactions. In this study, we employed an adaptation paradigm to examine the mechanisms underlying the perception of another''s gaze. Previous research has shown that the interleaved presentation of leftwards and rightwards gazing adaptor stimuli results in observers judging a wider range of gaze deviations as being direct. We applied a similar paradigm to examine how human observers encode oblique (e.g. upwards and to the left) directions of gaze. We presented observers with interleaved gaze adaptors and examined whether adaptation differed between congruent (adaptor and test along same axis) and incongruent conditions. We find greater adaptation in congruent conditions along cardinal (horizontal and vertical) and non-cardinal (oblique) directions suggesting gaze is not coded alone by cardinal mechanisms. Our results suggest that the functional aspects of gaze processing might parallel that of basic visual features such as orientation.     

Covert tracking: a combined ERP and fixational eye movement study

Attention can be directed to particular spatial locations, or to objects that appear at anticipated points in time. While most work has focused on spatial or temporal attention in isolation, we investigated covert tracking of smoothly moving objects, which requires continuous coordination of both. We tested two propositions about the neural and cognitive basis of this operation: first that covert tracking is a right hemisphere function, and second that pre-motor components of the oculomotor system are responsible for driving covert spatial attention during tracking. We simultaneously recorded event related potentials (ERPs) and eye position while participants covertly tracked dots that moved leftward or rightward at 12 or 20°/s. ERPs were sensitive to the direction of target motion. Topographic development in the leftward motion was a mirror image of the rightward motion, suggesting that both hemispheres contribute equally to covert tracking. Small shifts in eye position were also lateralized according to the direction of target motion, implying covert activation of the oculomotor system. The data addresses two outstanding questions about the nature of visuospatial tracking. First, covert tracking is reliant upon a symmetrical frontoparietal attentional system, rather than being right lateralized. Second, this same system controls both pursuit eye movements and covert tracking.     

On the directional sensitivity of motion detectors

The output of a motion detector depends on the direction of pattern motion, relative to the axis defined by its two input elements. Usually a cosine shaped directional sensitivity characteristics is assumed: The response is strongest for pattern motion along the detector axis, reversing its sign for motion in opposite direction; for motion perpendicular to the detector axis it is expected to be zero, with intermediate values for oblique motion directions. However, geometric considerations show that this expectation is by no means trivial. When a periodic pattern moves along a direction a relative to the detector axis, the spatiotemporal intensity distribution along the detector axis can be described by its apparent spatial wavelength and its apparent velocity, which both vary with 1/cos. In consequence, a motion detector depending exclusively on the apparent velocity of the stimulus would respond strongest to gratings moving perpendicular to the detector axis, whereas motion along the detector axis would yield the smallest response in such a detector. The response of a motion detector of the correlation type, on the other hand, is determined by the ratio between velocity and wavelength, the temporal frequency, which is not influenced by the direction of pattern motion, and by the ratio between sampling base and the wavelength. The latter feature leads to a cosine-shaped directional characteristics for large pattern wavelengths. However, for smaller wavelengths specific deviations from a simple harmonic are expected. These expectations were confirmed by the simulation of an elementary motion detector model and extended for a slightly more elaborated model. Representing a biological motion detecting unit of the correlation type, the directional characteristics of the H1 interneuron in the fly's brain was investigated electrophysiologically, and compared to the simulations.     

Tuning Properties of MT and MSTd and Divisive Interactions for Eye-Movement Compensation

The primate brain intelligently processes visual information from the world as the eyes move constantly. The brain must take into account visual motion induced by eye movements, so that visual information about the outside world can be recovered. Certain neurons in the dorsal part of monkey medial superior temporal area (MSTd) play an important role in integrating information about eye movements and visual motion. When a monkey tracks a moving target with its eyes, these neurons respond to visual motion as well as to smooth pursuit eye movements. Furthermore, the responses of some MSTd neurons to the motion of objects in the world are very similar during pursuit and during fixation, even though the visual information on the retina is altered by the pursuit eye movement. We call these neurons compensatory pursuit neurons. In this study we develop a computational model of MSTd compensatory pursuit neurons based on physiological data from single unit studies. Our model MSTd neurons can simulate the velocity tuning of monkey MSTd neurons. The model MSTd neurons also show the pursuit compensation property. We find that pursuit compensation can be achieved by divisive interaction between signals coding eye movements and signals coding visual motion. The model generates two implications that can be tested in future experiments: (1) compensatory pursuit neurons in MSTd should have the same direction preference for pursuit and retinal visual motion; (2) there should be non-compensatory pursuit neurons that show opposite preferred directions of pursuit and retinal visual motion.     

Beta,but Not Gamma,Band Oscillations Index Visual Form-Motion Integration

Electrophysiological oscillations in different frequency bands co-occur with perceptual, motor and cognitive processes but their function and respective contributions to these processes need further investigations. Here, we recorded MEG signals and seek for percept related modulations of alpha, beta and gamma band activity during a perceptual form/motion integration task. Participants reported their bound or unbound perception of ambiguously moving displays that could either be seen as a whole square-like shape moving along a Lissajou''s figure (bound percept) or as pairs of bars oscillating independently along cardinal axes (unbound percept). We found that beta (15–25 Hz), but not gamma (55–85 Hz) oscillations, index perceptual states at the individual and group level. The gamma band activity found in the occipital lobe, although significantly higher during visual stimulation than during base line, is similar in all perceptual states. Similarly, decreased alpha activity during visual stimulation is not different for the different percepts. Trial-by-trial classification of perceptual reports based on beta band oscillations was significant in most observers, further supporting the view that modulation of beta power reliably index perceptual integration of form/motion stimuli, even at the individual level.     

脑光学成像技术揭示的猫初级视皮层方位倾斜效应

方位倾斜效应（ｏｂｌｉｑｕｅ ｅｆｆｅｃｔ）是人类普遍存在的视觉心理效应。为了检测其神经基础,我们采用脑光学成像方法,对猫初级视觉皮层较大范围内的水平－垂直方位光栅刺激敏感区和倾斜方位光栅刺激敏感区的大小及其反应强度进行了定量分析。结果表明：水平－垂直敏感区比倾斜角敏感区面积大,平均差异为４．７％;水平－垂直方位刺激引起的反应强度整体上比倾斜角方位刺激大。以上结果澄清了以往一些电生理研究结果的不同     

Smooth Pursuit and Visual Occlusion: Active Inference and Oculomotor Control in Schizophrenia

This paper introduces a model of oculomotor control during the smooth pursuit of occluded visual targets. This model is based upon active inference, in which subjects try to minimise their (proprioceptive) prediction error based upon posterior beliefs about the hidden causes of their (exteroceptive) sensory input. Our model appeals to a single principle – the minimisation of variational free energy – to provide Bayes optimal solutions to the smooth pursuit problem. However, it tries to accommodate the cardinal features of smooth pursuit of partially occluded targets that have been observed empirically in normal subjects and schizophrenia. Specifically, we account for the ability of normal subjects to anticipate periodic target trajectories and emit pre-emptive smooth pursuit eye movements – prior to the emergence of a target from behind an occluder. Furthermore, we show that a single deficit in the postsynaptic gain of prediction error units (encoding the precision of posterior beliefs) can account for several features of smooth pursuit in schizophrenia: namely, a reduction in motor gain and anticipatory eye movements during visual occlusion, a paradoxical improvement in tracking unpredicted deviations from target trajectories and a failure to recognise and exploit regularities in the periodic motion of visual targets. This model will form the basis of subsequent (dynamic causal) models of empirical eye tracking measurements, which we hope to validate, using psychopharmacology and studies of schizophrenia.     

Incorporating Prediction in Models for Two-Dimensional Smooth Pursuit

A predictive component can contribute to the command signal for smooth pursuit. This is readily demonstrated by the fact that low frequency sinusoidal target motion can be tracked with zero time delay or even with a small lead. The objective of this study was to characterize the predictive contributions to pursuit tracking more precisely by developing analytical models for predictive smooth pursuit. Subjects tracked a small target moving in two dimensions. In the simplest case, the periodic target motion was composed of the sums of two sinusoidal motions (SS), along both the horizontal and the vertical axes. Motions following the same or similar paths, but having a richer spectral composition, were produced by having the target follow the same path but at a constant speed (CS), and by combining the horizontal SS velocity with the vertical CS velocity and vice versa. Several different quantitative models were evaluated. The predictive contribution to the eye tracking command signal could be modeled as a low-pass filtered target acceleration signal with a time delay. This predictive signal, when combined with retinal image velocity at the same time delay, as in classical models for the initiation of pursuit, gave a good fit to the data. The weighting of the predictive acceleration component was different in different experimental conditions, being largest when target motion was simplest, following the SS velocity profiles.     

Seeing objects in motion

This paper reports estimates of the conjoint spatiotemporal tuning functions of the neural mechanisms of the human vision system which detect image motion. The functions were derived from measurements of the minimum contrast necessary to detect the direction of drift of a sinusoidal grating, in the presence of phase-reversed masking gratings of various spatial and temporal frequencies. A mask of similar spatial and temporal frequencies to the test grating reduces sensitivity considerably, whereas one differing greatly in spatial or temporal frequency has little or no effect. The results show that for test gratings drifting at 8 Hz, the tuning function is bandpass in both space and time, peaked at the temporal and spatial frequency (SF) of the test (SFs were 0.1, 1 or 5 c deg-1; c represents cycles throughout). For a grating of 5 c deg-1 drifting at 0.3 Hz, the function is bandpass in space but lowpass in time. Fourier transform of the frequency results yields a function in space-time which we term the 'spatiotemporal receptive field'. For movement detectors (bandpass in space and time) the fields comprise alternating ridges of opposing polarity, elongated in space-time along the preferred velocity axis of the detector. We suggest that this organization explains how detectors analyse form and motion concurrently and accounts, at least in part, for a variety of perceptual phenomena, including summation, reduction of motion smear, metacontrast, stroboscopic motion and spatiotemporal interpolation.     

Anticipatory Smooth Eye Movements in Autism Spectrum Disorder

Smooth pursuit eye movements are important for vision because they maintain the line of sight on targets that move smoothly within the visual field. Smooth pursuit is driven by neural representations of motion, including a surprisingly strong influence of high-level signals representing expected motion. We studied anticipatory smooth eye movements (defined as smooth eye movements in the direction of expected future motion) produced by salient visual cues in a group of high-functioning observers with Autism Spectrum Disorder (ASD), a condition that has been associated with difficulties in either generating predictions, or translating predictions into effective motor commands. Eye movements were recorded while participants pursued the motion of a disc that moved within an outline drawing of an inverted Y-shaped tube. The cue to the motion path was a visual barrier that blocked the untraveled branch (right or left) of the tube. ASD participants showed strong anticipatory smooth eye movements whose velocity was the same as that of a group of neurotypical participants. Anticipatory smooth eye movements appeared on the very first cued trial, indicating that trial-by-trial learning was not responsible for the responses. These results are significant because they show that anticipatory capacities are intact in high-functioning ASD in cases where the cue to the motion path is highly salient and unambiguous. Once the ability to generate anticipatory pursuit is demonstrated, the study of the anticipatory responses with a variety of types of cues provides a window into the perceptual or cognitive processes that underlie the interpretation of events in natural environments or social situations.     

Kinematics of Visually-Guided Eye Movements

One of the hallmarks of an eye movement that follows Listing’s law is the half-angle rule that says that the angular velocity of the eye tilts by half the angle of eccentricity of the line of sight relative to primary eye position. Since all visually-guided eye movements in the regime of far viewing follow Listing’s law (with the head still and upright), the question about its origin is of considerable importance. Here, we provide theoretical and experimental evidence that Listing’s law results from a unique motor strategy that allows minimizing ocular torsion while smoothly tracking objects of interest along any path in visual space. The strategy consists in compounding conventional ocular rotations in meridian planes, that is in horizontal, vertical and oblique directions (which are all torsion-free) with small linear displacements of the eye in the frontal plane. Such compound rotation-displacements of the eye can explain the kinematic paradox that the fixation point may rotate in one plane while the eye rotates in other planes. Its unique signature is the half-angle law in the position domain, which means that the rotation plane of the eye tilts by half-the angle of gaze eccentricity. We show that this law does not readily generalize to the velocity domain of visually-guided eye movements because the angular eye velocity is the sum of two terms, one associated with rotations in meridian planes and one associated with displacements of the eye in the frontal plane. While the first term does not depend on eye position the second term does depend on eye position. We show that compounded rotation - displacements perfectly predict the average smooth kinematics of the eye during steady- state pursuit in both the position and velocity domain.