The precision of signals encoding active self-movement.

Everyday actions like moving the head, walking around and grasping objects are typically self-controlled. This presents a problem when studying the signals encoding such actions because active self-movement is difficult to control experimentally. Available techniques demand repeatable trials, but each action is unique, making it difficult to measure fundamental properties like psychophysical thresholds. We present a novel paradigm that recovers both precision and bias of self-movement signals with minimal constraint on the participant. The paradigm relies on linking image motion to previous self-movement, and two experimental phases to extract the signal encoding the latter. The paradigm takes care of a hidden source of external noise not previously accounted for in techniques that link display motion to self-movement in real time (e.g. virtual reality). We use head rotations as an example of self-movement, and show that the precision of the signals encoding head movement depends on whether they are being used to judge visual motion or auditory motion. We find that perceived motion is slowed during head movement in both cases. The 'non-image' signals encoding active head rotation (motor commands, proprioception and vestibular cues) are therefore biased towards lower speeds and/or displacements. In a second experiment, we trained participants to rotate their heads at different rates and found that the imprecision of the head rotation signal rises proportionally with head speed (Weber's Law). We discuss the findings in terms of the different motion cues used by vision and hearing, and the implications they have for Bayesian models of motion perception.

The pinna enhances angular discrimination in the frontal hemifield.

Human sound localization in the horizontal dimension is thought to be dominated by binaural cues, particularly interaural time delays, because monaural localization in this dimension is relatively poor. Remaining ambiguities of front versus back and up versus down are distinguished by high-frequency spectral cues generated by the pinna. The experiments in this study show that this account is incomplete. Using binaural listening throughout, the pinna substantially enhanced horizontal discrimination in the frontal hemifield, making discrimination in front better than discrimination at the rear, particularly for directions away from the median plane. Eliminating acoustic effects of the pinna by acoustically bypassing them or low-pass filtering abolished the advantage at the front without affecting the rear. Acoustic measurements revealed a pinna-induced spectral prominence that shifts smoothly in frequency as sounds move from 0° to 90° azimuth. The improved performance is discussed in terms of the monaural and binaural changes induced by the pinna.

Insufficient compensation for self-motion during perception of object speed: The vestibular Aubert-Fleischl phenomenon.

To estimate object speed with respect to the self, retinal signals must be summed with extraretinal signals that encode the speed of eye and head movement. Prior work has shown that differences in perceptual estimates of object speed based on retinal and oculomotor signals lead to biased percepts such as the Aubert-Fleischl phenomenon (AF), in which moving targets appear slower when pursued. During whole-body movement, additional extraretinal signals, such as those from the vestibular system, may be used to transform object speed estimates from a head-centered to a world-centered reference frame. Here we demonstrate that whole-body pursuit in the form of passive yaw rotation, which stimulates the semicircular canals of the vestibular system, leads to a slowing of perceived object speed similar to the classic oculomotor AF. We find that the magnitude of the vestibular and oculomotor AF is comparable across a range of speeds, despite the different types of input signal involved. This covariation might hint at a common modality-independent mechanism underlying the AF in both cases.

Bayesian Models of Individual Differences.

According to Bayesian models, perception and cognition depend on the optimal combination of noisy incoming evidence with prior knowledge of the world. Individual differences in perception should therefore be jointly determined by a person's sensitivity to incoming evidence and his or her prior expectations. It has been proposed that individuals with autism have flatter prior distributions than do nonautistic individuals, which suggests that prior variance is linked to the degree of autistic traits in the general population. We tested this idea by studying how perceived speed changes during pursuit eye movement and at low contrast. We found that individual differences in these two motion phenomena were predicted by differences in thresholds and autistic traits when combined in a quantitative Bayesian model. Our findings therefore support the flatter-prior hypothesis and suggest that individual differences in prior expectations are more systematic than previously thought. In order to be revealed, however, individual differences in sensitivity must also be taken into account.

Evidence that smooth pursuit velocity, not eye position, modulates alpha and beta oscillations in human middle temporal cortex.

Suppression of 5-25 Hz oscillations have been observed in MT+ during pursuit eye movements, suggesting oscillations that play a role in oculomotor control and/or the integration of extraretinal signals during pursuit. The amplitude of these rhythms appears to covary with head-centered eye position, but an alternative is that they depend on a velocity signal that lags the movement of the eyes. To investigate, we explored how alpha and beta amplitude changes related to ongoing eye movement depended on pursuit at different eccentricities. The results revealed largely identical patterns of modulation in the alpha and beta amplitude, irrespective of the eccentricity at which the pursuit eye movement was performed. The signals we measured therefore do not depend on head-centered position. A second experiment was designed to investigate whether the alpha and beta oscillations depended on the direction of pursuit, as opposed to just speed. We found no evidence that alpha or beta oscillations depended on direction, but there was a significant effect of eye speed on the magnitude of the beta suppression. This suggests distinct functional roles for alpha and beta suppression in pursuit behavior.

Saccadic compensation for reflexive optokinetic nystagmus just as good as compensation for volitional pursuit.

The natural viewing behavior of moving observers ideally requires target-selecting saccades to be coordinated with automatic gaze-stabilizing eye movements such as optokinetic nystagmus. However, it is unknown whether saccade plans can compensate for reflexive movement of the eye during the variable saccade latency period, and it is unclear whether reflexive nystagmus is even accompanied by extraretinal signals carrying the eye movement information that could potentially underpin such compensation. We show that saccades do partially compensate for optokinetic nystagmus that displaces the eye during the saccade latency period. Moreover, this compensation is as good as for displacements due to voluntary smooth pursuit. In other words, the saccade system appears to be as well coordinated with reflexive nystagmus as it is with volitional pursuit, which in turn implies that extraretinal signals accompany nystagmus and are just as informative as those accompanying pursuit.

Cortical oscillatory changes in human middle temporal cortex underlying smooth pursuit eye movements.

Extra-striate regions are thought to receive non-retinal signals from the pursuit system to maintain perceptual stability during eye movements. Here, we used magnetoencephalography (MEG) to study changes in oscillatory power related to smooth pursuit in extra-striate visual areas under three conditions: 'pursuit' of a small target, 'retinal motion' of a large background and 'pursuit + retinal motion' combined. All stimuli moved sinusoidally. MEG source reconstruction was performed using synthetic aperture magnetometry. Broadband alpha-beta suppression (5-25 Hz) was observed over bilateral extra-striate cortex (consistent with middle temporal cortex (MT+)) during all conditions. A functional magnetic resonance imaging study using the same experimental protocols confirmed an MT+ localisation of this extra-striate response. The alpha-beta envelope power in the 'pursuit' condition showed a hemifield-dependent eye-position signal, such that the global minimum in the alpha-beta suppression recorded in extra-striate cortex was greatest when the eyes were at maximum contralateral eccentricity. The 'retinal motion' condition produced sustained alpha-beta power decreases for the duration of stimulus motion, while the 'pursuit + retinal motion' condition revealed a double-dip 'W' shaped alpha-beta envelope profile with the peak suppression contiguous with eye position when at opposing maximum eccentricity. These results suggest that MT+ receives retinal as well as extra-retinal signals from the pursuit system as part of the process that enables the visual system to compensate for retinal motion during eye movement. We speculate that the suppression of the alpha-beta rhythm reflects either the integration of an eye position-dependent signal or one that lags the peak velocity of the sinusoidally moving target.

Horizontal fixation point oscillation and simulated viewpoint oscillation both increase vection in depth.

Previous research has shown that vection can be enhanced by adding horizontal simulated viewpoint oscillation to radial flow. Adding a horizontally oscillating fixation target to purely radial flow induces a superficially similar illusion of self-motion, where the observer's perceived heading oscillates left and right as their eyes pursue the moving target. This study directly compared the vection induced by these two conditions for the first time. Adding fixation point oscillation and simulated viewpoint oscillation to radial flow were both found to improve vection (relative to no oscillation control displays). Neither vection advantage could be explained in terms of differences in perceived scene rigidity or motion adaptation. Our findings also provided little support for the notion that pursuit eye-movements were essential for the simulated viewpoint oscillation advantage for vection (since observers successfully fixated a stationary, centrally- placed target during these conditions in the current experiments). The strongest support was found for the proposal that fixation point oscillation and simulated viewpoint oscillation both improve vection by increasing the observer's global retinal motion.

Perceived speed at low luminance: Lights out for the Bayesian observer?

To account for perceptual bias, Bayesian models use the precision of early sensory measurements to weight the influence of prior expectations. As precision decreases, prior expectations start to dominate. Important examples come from motion perception, where the slow-motion prior has been used to explain a variety of motion illusions in vision, hearing, and touch, many of which correlate appropriately with threshold measures of underlying precision. However, the Bayesian account seems defeated by the finding that moving objects appear faster in the dark, because most motion thresholds are worse at low luminance. Here we show this is not the case for speed discrimination. Our results show that performance improves at low light levels by virtue of a perceived contrast cue that is more salient in the dark. With this cue removed, discrimination becomes independent of luminance. However, we found perceived speed still increased in the dark for the same observers, and by the same amount. A possible interpretation is that motion processing is therefore not Bayesian, because our findings challenge a key assumption these models make, namely that the accuracy of early sensory measurements is independent of basic stimulus properties like luminance. However, a final experiment restored Bayesian behaviour by adding external noise, making discrimination worse and slowing perceived speed down. Our findings therefore suggest that motion is processed in a Bayesian fashion but based on noisy sensory measurements that also vary in accuracy.

Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex.

Neuronal orientation selectivity has been shown in animal models to require corticocortical network cooperation and to be dependent on the presence of GABAergic inhibition. However, it is not known whether variability in these fundamental neurophysiological parameters leads to variability in behavioral performance. Here, using a combination of magnetic resonance spectroscopy, magnetoencephalography, and visual psychophysics, we show that individual performance on a visual orientation discrimination task is correlated with both the resting concentration of GABA and the frequency of stimulus-induced gamma oscillations in human visual cortex. Behaviorally, a strong oblique effect was found, with the mean angular threshold for oblique discrimination being five times higher than that for vertically oriented stimuli. Similarly, we found an oblique effect for the dependency of performance on neurophysiological parameters. Orientation detection thresholds were significantly negatively correlated with visual cortex GABA concentration for obliquely oriented patterns (r = -0.65, p < 0.015) but did not reach significance for vertically oriented stimuli (r = -0.39, p = 0.2). Similarly, thresholds for obliquely oriented stimuli were negatively correlated with gamma oscillation frequency (r = -0.65, p < 0.017), but thresholds for vertical orientations were not (r = -0.02, p = 0.9). Gamma oscillation frequency was positively correlated with GABA concentration in primary visual cortex (r = 0.67, p < 0.013). These results confirm the importance of GABAergic inhibition in orientation selectivity and demonstrate, for the first time, that interindividual performance on a simple visual task is linked to neurotransmitter concentration. The results also suggest a key role for GABAergic gamma oscillations in visual discrimination tasks.

Extra-retinal vision: firing at will.

Recent evidence suggests that a key visual motion centre in the brain ignores extra-retinal motor information concerning reflexive eye movement. Instead it seems that neurons sensitive to oculomotor actions in this area fire at will.

Precision and accuracy of ocular following: influence of age and type of eye movement.

Previous work on ocular-following emphasises the accuracy of tracking eye movements. However, a more complete understanding of oculomotor control should account for variable error as well. We identify two forms of precision: 'shake', occurring over shorter timescales; 'drift', occurring over longer timescales. We show how these can be computed across a series of eye movements (e.g. a sequence of slow-phases or collection of pursuit trials) and then measure accuracy and precision for younger and older observers executing different types of eye movement. Overall, we found older observers were less accurate over a range of stimulus speeds and less precise at faster eye speeds. Accuracy declined more steeply for reflexive eye movements and shake was independent of speed. In all other instances, the two measures of precision expanded non-linearly with mean eye speed. We also found that shake during fixation was similar to shake for reflexive eye movement. The results suggest that deliberate and reflexive eye movement do not share a common non-linearity or a common noise source. The relationship of our data to previous studies is discussed, as are the consequences of imprecise eye movement for models of oculomotor control and perception during eye movement.

Discrimination contours for the perception of head-centered velocity.

There is little direct psychophysical evidence that the visual system contains mechanisms tuned to head-centered velocity when observers make a smooth pursuit eye movement. Much of the evidence is implicit, relying on measurements of bias (e.g., matching and nulling). We therefore measured discrimination contours in a space dimensioned by pursuit target motion and relative motion between target and background. Within this space, lines of constant head-centered motion are parallel to the main negative diagonal, so judgments dominated by mechanisms that combine individual components should produce contours with a similar orientation. Conversely, contours oriented parallel to the cardinal axes of the space indicate judgments based on individual components. The results provided evidence for mechanisms tuned to head-centered velocity-discrimination ellipses were significantly oriented away from the cardinal axes, toward the main negative diagonal. However, ellipse orientation was considerably less steep than predicted by a pure combination of components. This suggests that observers used a mixture of two strategies across trials, one based on individual components and another based on their sum. We provide a model that simulates this type of behavior and is able to reproduce the ellipse orientations we found.

Humans do not have direct access to retinal flow during walking.

Perceived visual speed has been reported to be reduced during walking. This reduction has been attributed to a partial subtraction of walking speed from visual speed (F. H. Durgin & K. Gigone, 2007; F. H. Durgin, K. Gigone, & R. Scott, 2005). We tested whether observers still have access to the retinal flow before subtraction takes place. Observers performed a 2IFC visual speed discrimination task while walking on a treadmill. In one condition, walking speed was identical in the two intervals, while in a second condition walking speed differed between intervals. If observers have access to the retinal flow before subtraction, any changes in walking speed across intervals should not affect their ability to discriminate retinal flow speed. Contrary to this "direct access hypothesis," we found that observers were worse at discrimination when walking speed differed between intervals. The results therefore suggest that observers do not have access to retinal flow before subtraction. We also found that the amount of subtraction depended on the visual speed presented, suggesting that the interaction between the processing of visual input and of self-motion is more complex than previously proposed.

Two-Dimensional Analysis of Horizontal and Vertical Pursuit in Infantile Nystagmus Reveals Quantitative Deficits in Accuracy and Precision.

Purpose: Infantile nystagmus (IN) presents with continuous, predominantly horizontal eye oscillations. It remains controversial whether those with IN have normal horizontal pursuit, while vertical pursuit has rarely been studied. We examined whether there are pursuit deficits associated with IN by investigating the effect of target direction, velocity, and amplitude. Methods: Twelve adults with idiopathic IN performed a pursuit task, a 0.4° dot moved either horizontally or vertically at 8 or 16°/s, through amplitudes of 8°, 16°, or 32°. Accuracy and precision errors were computed as bivariate probability density functions of target-relative eye velocities. Results: Eye velocity was less precise along the horizontal axis during both horizontal and vertical pursuit, reflecting the primary axis of the eye oscillation. Mean accuracy error along the target trajectory during vertical pursuit was just as impaired as during horizontal pursuit. There was a greater error in accuracy along the target trajectory for 16°/s targets than 8°/s. Finally, targets that oscillated at 2.0 Hz had a greater error in accuracy along the target trajectory than frequencies of 1.0 Hz or 0.5 Hz. When studied using the same experimental protocol, pursuit performance for typical observers was always better. Conclusions: These findings strongly support our hypothesis of severe deficits in pursuit accuracy in observers with IN for horizontally and vertically moving targets, as well as for targets that move at higher speeds or oscillate more quickly. Overall, IN pursuit impairment appears to have previously been underestimated, highlighting a need for further quantitative studies of dynamic visual function in those with IN.

Oscillatory, Computational, and Behavioral Evidence for Impaired GABAergic Inhibition in Schizophrenia.

The dysconnection hypothesis of schizophrenia (SZ) proposes that psychosis is best understood in terms of aberrant connectivity. Specifically, it suggests that dysconnectivity arises through aberrant synaptic modulation associated with deficits in GABAergic inhibition, excitation-inhibition balance and disturbances of high-frequency oscillations. Using a computational model combined with a graded-difficulty visual orientation discrimination paradigm, we demonstrate that, in SZ, perceptual performance is determined by the balance of excitation-inhibition in superficial cortical layers. Twenty-eight individuals with a DSM-IV diagnosis of SZ, and 30 age- and gender-matched healthy controls participated in a psychophysics orientation discrimination task, a visual grating magnetoencephalography (MEG) recording, and a magnetic resonance spectroscopy (MRS) scan for GABA. Using a neurophysiologically informed model, we quantified group differences in GABA, gamma measures, and the predictive validity of model parameters for orientation discrimination in the SZ group. MEG visual gamma frequency was reduced in SZ, with lower peak frequency associated with more severe negative symptoms. Orientation discrimination performance was impaired in SZ. Dynamic causal modeling of the MEG data showed that local synaptic connections were reduced in SZ and local inhibition correlated negatively with the severity of negative symptoms. The effective connectivity between inhibitory interneurons and superficial pyramidal cells predicted orientation discrimination performance within the SZ group; consistent with graded, behaviorally relevant, disease-related changes in local GABAergic connections. Occipital GABA levels were significantly reduced in SZ but did not predict behavioral performance or oscillatory measures. These findings endorse the importance, and behavioral relevance, of GABAergic synaptic disconnection in schizophrenia that underwrites excitation-inhibition balance.

Do we have direct access to retinal image motion during smooth pursuit eye movements?

One way the visual system estimates object motion during pursuit is to combine estimates of eye velocity and retinal motion. This questions whether observers need direct access to retinal motion during pursuit. We tested this idea by varying the correlation between retinal motion and objective motion in a two-interval speed discrimination task. Responses were classified according to three motion cues: retinal speed (based on measured eye movements), objective speed, and the relative motion between pursuit target and stimulus. In the first experiment, feedback was based on relative motion and this cue fit the response curves best. In the second experiment, simultaneous relative motion was removed but observers still used the sequential relative motion between pursuit target and dot pattern to make their judgements. In a final experiment, feedback was given explicitly on the retinal motion, using online measurements of eye movements. Nevertheless, sequential relative motion still provided the best account of the data. The results suggest that observers do not have direct access to retinal motion when making perceptual judgements about movement during pursuit.

Two-Dimensional Analysis of Smooth Pursuit Eye Movements Reveals Quantitative Deficits in Precision and Accuracy.

PURPOSE: Small moving targets are followed by pursuit eye movements, with success ubiquitously defined by gain. Gain quantifies accuracy, rather than precision, and only for eye movements along the target trajectory. Analogous to previous studies of fixation, we analyzed pursuit performance in two dimensions as a function of target direction, velocity, and amplitude. As a subsidiary experiment, we compared pursuit performance against that of fixation. METHODS: Eye position was recorded from 15 observers during pursuit. The target was a 0.4° dot that moved across a large screen at 8°/s or 16°/s, either horizontally or vertically, through peak-to-peak amplitudes of 8°, 16°, or 32°. Two-dimensional eye velocity was expressed relative to the target, and a bivariate probability density function computed to obtain accuracy and precision. As a comparison, identical metrics were derived from fixation data. RESULTS: For all target directions, eye velocity was less precise along the target trajectory. Eye velocities orthogonal to the target trajectory were more accurate during vertical pursuit than horizontal. Pursuit accuracy and precision along and orthogonal to the target trajectory decreased at the higher target velocity. Accuracy along the target trajectory decreased with smaller target amplitudes. CONCLUSIONS: Orthogonal to the target trajectory, pursuit was inaccurate and imprecise. Compared to fixation, pursuit was less precise and less accurate even when following the stimulus that gave the best performance. TRANSLATIONAL RELEVANCE: This analytical approach may help the detection of subtle deficits in slow phase eye movements that could be used as biomarkers for disease progression and/or treatment.

Motion perception during sinusoidal smooth pursuit eye movements: signal latencies and non-linearities.

Smooth pursuit eye movements add motion to the retinal image. To compensate, the visual system can combine estimates of pursuit velocity and retinal motion to recover motion with respect to the head. Little attention has been paid to the temporal characteristics of this compensation process. Here, we describe how the latency difference between the eye movement signal and the retinal signal can be measured for motion perception during sinusoidal pursuit. In two experiments, observers compared the peak velocity of a motion stimulus presented in pursuit and fixation intervals. Both the pursuit target and the motion stimulus moved with a sinusoidal profile. The phase and amplitude of the motion stimulus were varied systematically in different conditions, along with the amplitude of pursuit. The latency difference between the eye movement signal and the retinal signal was measured by fitting the standard linear model and a non-linear variant to the observed velocity matches. We found that the eye movement signal lagged the retinal signal by a small amount. The non-linear model fitted the velocity matches better than the linear one and this difference increased with pursuit amplitude. The results support previous claims that the visual system estimates eye movement velocity and retinal velocity in a non-linear fashion and that the latency difference between the two signals is small.

A preference for visual speed during smooth pursuit eye movement.

Does the preference for visual speed extend to motion perception when the eye moves? Current evidence from psychophysics and neuroscience is limited to small patches of image motion and stationary fixation. Active observers, however, are more likely to use large patches of retinal flow and extraretinal signals accompanying eye movement to judge motion. We therefore investigated whether speed remains a primary dimension during smooth pursuit using a "discrimination-contour" technique. Our results showed that observers struggled most when trying to discriminate pursued stimuli that traveled at the same speed but moved over different distances and durations. This remained the case when retinal flow was added, and when we isolated trials in which extraretinal signals were the only salient cue to motion. Our results suggest that preferential sensitivity for visual speed is quite general, supported by the many different types of motion mechanism used by active observers. (PsycINFO Database Record (c) 2018 APA, all rights reserved).