Extraretinal Signals Research Articles

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.

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).

Real-motion signals in human early visual cortex

Eye movements induce visual motion that can complicate the stable perception of the world. The visual system compensates for such self-induced visual motion by integrating visual input with efference copies of eye movement commands. This mechanism is central as it does not only support perceptual stability but also mediates reliable perception of world-centered objective motion. In humans, it remains elusive whether visual motion responses in early retinotopic cortex are driven by objective motion or by retinal motion associated with it. To address this question, we used fMRI to examine functional responses of sixteen visual areas to combinations of planar objective motion and pursuit eye movements. Observers were exposed to objective motion that was faster, matched or slower relative to pursuit, allowing us to compare conditions that differed in objective motion velocity while retinal motion and eye movement signals were matched. Our results show that not only higher level motion regions such as V3A and V6, but also early visual areas signaled the velocity of objective motion, hence the product of integrating retinal with non-retinal signals. These results shed new light on mechanisms that mediate perceptual stability and real-motion perception, and show that extra-retinal signals related to pursuit eye movements influence processing in human early visual cortex.

Integration of visual and non-visual self-motion cues during voluntary head movements in the human brain

Our phenomenological experience of the stable world is maintained by continuous integration of visual self-motion with extra-retinal signals. However, due to conventional constraints of fMRI acquisition in humans, neural responses to visuo-vestibular integration have only been studied using artificial stimuli, in the absence of voluntary head-motion. We here circumvented these limitations and let participants to move their heads during scanning. The slow dynamics of the BOLD signal allowed us to acquire neural signal related to head motion after the observer's head was stabilized by inflatable aircushions. Visual stimuli were presented on head-fixed display goggles and updated in real time as a function of head-motion that was tracked using an external camera. Two conditions simulated forward translation of the participant. During physical head rotation, the congruent condition simulated a stable world, whereas the incongruent condition added arbitrary lateral motion. Importantly, both conditions were precisely matched in visual properties and head-rotation. By comparing congruent with incongruent conditions we found evidence consistent with the multi-modal integration of visual cues with head motion into a coherent “stable world” percept in the parietal operculum and in an anterior part of parieto-insular cortex (aPIC). In the visual motion network, human regions MST, a dorsal part of VIP, the cingulate sulcus visual area (CSv) and a region in precuneus (Pc) showed differential responses to the same contrast. The results demonstrate for the first time neural multimodal interactions between precisely matched congruent versus incongruent visual and non-visual cues during physical head-movement in the human brain. The methodological approach opens the path to a new class of fMRI studies with unprecedented temporal and spatial control over visuo-vestibular stimulation.

Aperture Synthesis Shows Perceptual Integration of Geometrical Form Across Saccades.

We investigated the perceptual bias in perceived relative lengths in the Brentano version of the Müller-Lyer arrowheads figure. The magnitude of the bias was measured both under normal whole-figure viewing condition and under an aperture viewing condition, where participants moved their gaze around the figure but could see only one arrowhead at a time through a Gaussian-weighted contrast window. The extent of the perceptual bias was similar under the two conditions. The stimuli were presented on a CRT in a light-proof room with room-lights off, but visual context was provided by a rectangular frame surrounding the figure. The frame was either stationary with respect to the figure or moved in such a manner that the bias would be counteracted if the observer were locating features with respect to the frame. Biases were reduced in the latter condition. We conclude that integration occurs over saccades, but largely in an external visual framework, rather than in a body-centered frame using an extraretinal signal.

Response of pursuit cells in MST after eye position perturbation by microstimulation of the Superior Colliculus (SC)

Primates use the fovea to maintain high quality central vision of the world. When a target is moving, smooth pursuit eye movements (SEM) keep the fovea of both eyes on target. A large proportion of neurons in area MST discharge during SEM. These smooth pursuit cells (SPC) carry visual and extraretinal signals. We recorded 27 SPC in MST of a macaque monkey during SEM trials interrupted with a saccade that was elicited by electrical microstimulation (MS) in the SC. The MS consisted of a train of pulses (0.1ms, 400Hz, 40ms) at low currents (< 40mA). The tracking behavior was characterized by 1) an evoked saccade that brought the eye outside the target path, 2) a SEM following this abrupt change in eye position and 3) a corrective saccade. We quantified the ratio of activity after the evoked saccade, before the corrective saccade and during the corrective saccade. A majority of neurons (63%) presented ratios between 0.8 and 1.2 after the evoked saccade but ratios less than 0.8 during the corrective saccade. Among this subpopulation, 59% actually had a decrease of their firing rate before the corrective saccade. On average, this drop of activity occurred 54 (±11ms) after the evoked saccade offset or 109 (±9ms) after its onset. Interestingly, in 90% of cases the latency of this drop of activity was sensitive to the delay between the evoked and corrective saccades. Finally, 22% neurons did not present a drop of activity during these intervals while 15% presented a decrease from the evoked saccade offset. This eye position perturbation showed that the activity of a majority of MST smooth pursuit cells was not interrupted by a direct corollary discharge from the saccadic system. However this activity seems inhibited by the occurrence of a corrective saccade even though not always time-locked to it. Meeting abstract presented at VSS 2017

Saccadic suppression during voluntary versus reactive saccades.

Saccades are fast eye movements that reorient gaze. They can be performed voluntarily-for example, when viewing a scene-but they can also be triggered in reaction to suddenly appearing targets. The generation of these voluntary and reactive saccades have been shown to involve partially different cortical pathways. However, saccades of either type confront the visual system with a major challenge from massive image motion on the retina. Despite the fact that the whole scene is swept across the retina, a saccade usually does not elicit a percept of motion. This saccadic omission has been linked to a transient decrease of visual sensitivity during the eye movement, a phenomenon called saccadic suppression. A passive origin of saccadic suppression based on temporal masking has been proposed as well as an active central process that inhibits visual processing during the saccade. The latter one would need to include an extraretinal signal, which is generated already during saccade preparation. Since saccade generation differs for voluntary and reactive saccades, timing and nature of this extraretinal signal as well as its impact on visual sensitivity might also differ. We measured detection thresholds for luminance stimuli that were flashed during voluntary and reactive saccades and during fixation. Detection thresholds were higher during voluntary than during reactive saccades such that suppression appeared stronger during voluntary saccades. Stronger suppression in voluntary saccades could arise from a stronger extraretinal signal that activates suppression or could indicate that a suppression underlying process itself partially differs between voluntary and reactive saccades.

FEFsem neuronal response during combined volitional and reflexive pursuit.

Although much is known about volitional and reflexive smooth eye movements individually, much less is known about how they are coordinated. It is hypothesized that separate cortico-ponto-cerebellar loops subserve these different types of smooth eye movements. Specifically, the MT-MST-DLPN pathway is thought to be critical for ocular following eye movements, whereas the FEF-NRTP pathway is understood to be vital for volitional smooth pursuit. However, the role that these loops play in combined volitional and reflexive behavior is unknown. We used a large, textured background moving in conjunction with a small target spot to investigate the eye movements evoked by a combined volitional and reflexive pursuit task. We also assessed the activity of neurons in the smooth eye movement subregion of the frontal eye field (FEFsem). We hypothesized that the pursuit system would show less contribution from the volitional pathway in this task, owing to the increased involvement of the reflexive pathway. In accordance with this hypothesis, a majority of FEFsem neurons (63%) were less active during pursuit maintenance in a combined volitional and reflexive pursuit task than during purely volitional pursuit. Interestingly and surprisingly, the neuronal response to the addition of the large-field motion was highly correlated with the neuronal response to a target blink. This suggests that FEFsem neuronal responses to these different perturbations—whether the addition or subtraction of retinal input—may be related. We conjecture that these findings are due to changing weights of both the volitional and reflexive pathways, as well as retinal and extraretinal signals.

Where are you heading? Flexible integration of retinal and extra-retinal cues during self-motion perception.

As we move forward in the environment, we experience a radial expansion of the retinal image, wherein the center corresponds to the instantaneous direction of self-motion. Humans can precisely perceive their heading direction even when the retinal motion is distorted by gaze shifts due to eye/body rotations. Previous studies have suggested that both retinal and extra-retinal strategies can compensate for the retinal image distortion. However, the relative contributions of each strategy remain unclear. To address this issue, we devised a two-alternative-headings discrimination task, in which participants had either real or simulated pursuit eye movements. The two conditions had the same retinal input but either with or without extra-retinal eye movement signals. Thus, the behavioral difference between conditions served as a metric of extra-retinal contribution. We systematically and independently manipulated pursuit speed, heading speed, and the reliability of retinal signals. We found that the levels of extra-retinal contributions increased with increasing pursuit speed (stronger extra-retinal signal), and with decreasing heading speed (weaker retinal signal). In addition, extra-retinal contributions also increased as we corrupted retinal signals with noise. Our results revealed that the relative magnitude of retinal and extra-retinal contributions was not fixed but rather flexibly adjusted to each specific task condition. This task-dependent, flexible integration appears to take the form of a reliability-based weighting scheme that maximizes heading performance.

Stationary Objects Flashed Periodically Appear to Move During Smooth Pursuit Eye Movement.

We discovered that a white disc flashed twice at the same location appears to move during smooth pursuit eye tracking in the direction opposite to that of the eye movement. We called this novel phenomenon movement-induced apparent motion (MIAM). Using the method of constant stimuli, we measured the required displacement of the second appearance of the disc in the pursuit direction to null the effect during the closed-loop stage of smooth pursuit eye tracking. We observed a strong linear relationship between the points of subjective stationarity and the inter-stimuli intervals for four smooth pursuit eye movement speeds. The slopes and y-intercepts of these linear fits were well predicted by the hypothesis according to which subjects saw illusory motion from the first to the second retinal projections of the flashed disc during smooth pursuit eye movement, with no extra-retinal signal compensation.

Temporal dynamics of retinal and extraretinal signals in the FEFsem during smooth pursuit eye movements.

Neurons in the smooth eye movement subregion of the frontal eye field (FEFsem) are known to play an important role in voluntary smooth pursuit eye movements. Underlying this function are projections to parietal and prefrontal visual association areas and subcortical structures, all known to play vital but differing roles in the execution of smooth pursuit. Additionally, the FEFsem has been shown to carry a diverse array of signals (e.g., eye velocity, acceleration, gain control). We hypothesized that distinct subpopulations of FEFsem neurons subserve these diverse functions and projections, and that the relative weights of retinal and extraretinal signals could form the basis for categorization of units. To investigate this, we used a step-ramp tracking task with a target blink to determine the relative contributions of retinal and extraretinal signals in individual FEFsem neurons throughout pursuit. We found that the contributions of retinal and extraretinal signals to neuronal activity and behavior change throughout the time course of pursuit. A clustering algorithm revealed three distinct neuronal subpopulations: cluster 1 was defined by a higher sensitivity to eye velocity, acceleration, and retinal image motion; cluster 2 had greater activity during blinks; and cluster 3 had significantly greater eye position sensitivity. We also performed a comparison with a sample of medial superior temporal neurons to assess similarities and differences between the two areas. Our results indicate the utility of simple tests such as the target blink for parsing the complex and multifaceted roles of cortical areas in behavior.NEW & NOTEWORTHY The frontal eye field (FEF) is known to play a critical role in volitional smooth pursuit, carrying a variety of signals that are distributed throughout the brain. This study used a novel application of a target blink task during step ramp tracking to determine, in combination with a clustering algorithm, the relative contributions of retinal and extraretinal signals to FEF activity and the extent to which these contributions could form the basis for a categorization of neurons.

Auditory compensation for head rotation is incomplete.

Hearing is confronted by a similar problem to vision when the observer moves. The image motion that is created remains ambiguous until the observer knows the velocity of eye and/or head. One way the visual system solves this problem is to use motor commands, proprioception, and vestibular information. These “extraretinal signals” compensate for self-movement, converting image motion into head-centered coordinates, although not always perfectly. We investigated whether the auditory system also transforms coordinates by examining the degree of compensation for head rotation when judging a moving sound. Real-time recordings of head motion were used to change the “movement gain” relating head movement to source movement across a loudspeaker array. We then determined psychophysically the gain that corresponded to a perceptually stationary source. Experiment 1 showed that the gain was small and positive for a wide range of trained head speeds. Hence, listeners perceived a stationary source as moving slightly opposite to the head rotation, in much the same way that observers see stationary visual objects move against a smooth pursuit eye movement. Experiment 2 showed the degree of compensation remained the same for sounds presented at different azimuths, although the precision of performance declined when the sound was eccentric. We discuss two possible explanations for incomplete compensation, one based on differences in the accuracy of signals encoding image motion and self-movement and one concerning statistical optimization that sacrifices accuracy for precision. We then consider the degree to which such explanations can be applied to auditory motion perception in moving listeners.

The Role of Dopamine in Anticipatory Pursuit Eye Movements: Insights from Genetic Polymorphisms in Healthy Adults.

There is a long history of eye movement research in patients with psychiatric diseases for which dysfunctions of neurotransmission are considered to be the major pathologic mechanism. However, neuromodulation of oculomotor control is still hardly understood. We aimed to investigate in particular the impact of dopamine on smooth pursuit eye movements. Systematic variability in dopaminergic transmission due to genetic polymorphisms in healthy subjects offers a noninvasive opportunity to determine functional associations. We measured smooth pursuit in 110 healthy subjects genotyped for two well-documented polymorphisms, the COMT Val158Met polymorphism and the SLC6A3 3′-UTR-VNTR polymorphism. Pursuit paradigms were chosen to particularly assess the ability of the pursuit system to initiate tracking when target motion onset is blanked, reflecting the impact of extraretinal signals. In contrast, when following a fully visible target sensory, retinal signals are available. Our results highlight the crucial functional role of dopamine for anticipatory, but not for sensory-driven, pursuit processes. We found the COMT Val158Met polymorphism specifically associated with anticipatory pursuit parameters, emphasizing the dominant impact of prefrontal dopamine activity on complex oculomotor control. In contrast, modulation of striatal dopamine activity by the SLC6A3 3′-UTR-VNTR polymorphism had no significant functional effect. Though often neglected so far, individual differences in healthy subjects provide a promising approach to uncovering functional mechanisms and can be used as a bridge to understanding deficits in patients.

Saccade Preparation Reshapes Sensory Tuning

Human observers make large rapid eye movements-saccades-to bring behaviorally relevant information into the fovea, where spatial resolution is high. In some visual tasks [1-4], performance at the location of a saccade target improves before the eyes move. Although these findings provide evidence that extra-retinal signals evoked by saccades can enhance visual perception, it remains unknown whether and how presaccadic modulations change the processing of feature information and thus modulate visual representations. To answer this question, one must go beyond the use of methods that only probe performance accuracy (d') in different tasks. Here, using a psychophysical reverse correlation approach [5-8], we investigated how saccade preparation influences the processing of orientation and spatial frequency-two building blocks of early vision. We found that saccade preparation selectively enhanced the gain of high spatial frequency information and narrowed orientation tuning at the upcoming saccade landing position. These modulations were time locked to saccade onset, peaking right before the eyes moved (-50-0ms). Moreover, merely deploying covert attention within the same temporal interval without preparing a saccade did not alter performance. The observed presaccadic tuning changes may correspond to the presaccadic enhancement [9-11] and receptive field shifts reported in neurophysiological studies [12-14]. Saccade preparation may support transaccadic integration by reshaping the representation of the saccade target to be more fovea-like just before theeyes move. The presaccadic modulations on spatial frequency and orientation processing illustrate a strong perception-action coupling by revealing that the visual system dynamically reshapes feature selectivity contingent upon eye movements.

Joint representation of translational and rotational components of optic flow in parietal cortex

Terrestrial navigation naturally involves translations within the horizontal plane and eye rotations about a vertical (yaw) axis to track and fixate targets of interest. Neurons in the macaque ventral intraparietal (VIP) area are known to represent heading (the direction of self-translation) from optic flow in a manner that is tolerant to rotational visual cues generated during pursuit eye movements. Previous studies have also reported that eye rotations modulate the response gain of heading tuning curves in VIP neurons. We tested the hypothesis that VIP neurons simultaneously represent both heading and horizontal (yaw) eye rotation velocity by measuring heading tuning curves for a range of rotational velocities of either real or simulated eye movements. Three findings support the hypothesis of a joint representation. First, we show that rotation velocity selectivity based on gain modulations of visual heading tuning is similar to that measured during pure rotations. Second, gain modulations of heading tuning are similar for self-generated eye rotations and visually simulated rotations, indicating that the representation of rotation velocity in VIP is multimodal, driven by both visual and extraretinal signals. Third, we show that roughly one-half of VIP neurons jointly represent heading and rotation velocity in a multiplicatively separable manner. These results provide the first evidence, to our knowledge, for a joint representation of translation direction and rotation velocity in parietal cortex and show that rotation velocity can be represented based on visual cues, even in the absence of efference copy signals.

Ocular Fixation Abnormality in Patients with Autism Spectrum Disorder.

We examined the factors that influence ocular fixation control in adults with autism spectrum disorder (ASD) including sensory information, individuals' motor characteristics, and inhibitory control. The ASD group showed difficulty in maintaining fixation especially when there was no fixation target. The fixational eye movement characteristics of individuals were consistent regardless of the presence or absence of a fixation target in the controls, but not in the ASD group. Additionally, fixation stability did not correlate with an ability to suppress reflexive saccades measured by an antisaccade task. These findings suggest that ASD adults have deficits in converting alternative sensory information, such as retinal signals in the peripheral visual field or extraretinal signals, to motor commands when the foveal information is unavailable.

Perceiving a continuous visual world across voluntary eye blinks.

People blink their eyes every few seconds, but the changes in retinal illumination that accompany eyeblinks are hardly noticed. Furthermore, despite the loss of visual input, visual experience remains continuous across eyeblinks. Two hypotheses were investigated to account for these phenomena. The first proposes that perceptual information is maintained across a blink whereas the second proposes that perceptual information is not maintained but rather postblink perceptual experience is antedated to the beginning of the blink. Two experiments found no evidence for temporal antedating of a stimulus presented during a voluntary eyeblink. In a third experiment subjects judged the temporal duration of a stimulus that was interrupted by a voluntary eyeblink with that of a stimulus presented while the eyes were open. The duration of stimuli that were interrupted by eyeblinks was judged to be 117 ms shorter than that of stimuli presented while the eyes remained open, indicating that blink duration was not accounted for in the perception of stimulus duration. This suggests that perceptual experience is neither maintained nor antedated across eyeblinks, but rather is ignored, perhaps in response to the extraretinal signal that accompanies the eyeblink. (PsycINFO Database Record

Non-linear retinal processing supports invariance during fixational eye movements

Fixational eye movements can rapidly shift the retinal image, but typically remain unnoticed. We identify and simulate a model mechanism for the suppression of erroneous motion signals under fixational eye movements. This mechanism exploits the non-linearities common to many classes of large retinal ganglion cells in the mammalian retina, and negates the need for extra-retinal signals or explicit gaze information. When tested using natural images undergoing simulated fixational eye movements, our model successfully distinguishes “real world” motion from retinal motion induced by eye movements. In addition, this model suggests a possible explanation for several fixational eye movement related visual illusions such as the Ouchi–Spillmann and “Out-of-focus” illusions.

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 modulation of stimulus processing in primary visual cortex

Saccadic eye movements play a central role in primate vision. Yet, relatively little is known about their effects on the neural processing of visual inputs. Here we examine this question in primary visual cortex (V1) using receptive-field-based models, combined with an experimental design that leaves the retinal stimulus unaffected by saccades. This approach allows us to analyse V1 stimulus processing during saccades with unprecedented detail, revealing robust perisaccadic modulation. In particular, saccades produce biphasic firing rate changes that are composed of divisive gain suppression followed by an additive rate increase. Microsaccades produce similar, though smaller, modulations. We furthermore demonstrate that this modulation is likely inherited from the LGN, and is driven largely by extra-retinal signals. These results establish a foundation for integrating saccades into existing models of visual cortical stimulus processing, and highlight the importance of studying visual neuron function in the context of eye movements.