A revised analysis of the role of efference in motion perception

The analysis of motion perception historically has included efferent as well as afferent mechanisms to account for the perception of motion during eye movement. The application of efferent mechanisms to motion perception has been limited, however, by several illusions which are apparently inconsistent with the notion that oculomotor mechanisms contribute to motion perception. An alternative account is presented of the manner in which efference may contribute to the perception of motion. It is proposed that distinct smooth eye-movement systems contribute differentially to object motion perception. Specifically, activity in the smooth pursuit system gives rise to the perception of object motion, whereas activity in the smooth component of reflexive eye movements does not. Tracking of a moving object results in object motion perception as a result of efference in the pursuit system. However, the pursuit system may be activated to oppose the smooth component of reflexive eye movements in order to preserve fixation on a stationary object. In such cases neither the fixated object nor the eye is moving but illusory movement results from the efference in the pursuit system. A number of illusory movement phenomena are interpreted in terms of this model.     

Cognitive processes involved in smooth pursuit eye movements

Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.     

Cognitive processes involved in smooth pursuit eye movements

Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.     

Why eye movements and perceptual factors have to be controlled in studies on "representational momentum"

In order to study memory of the final position of a smoothly moving target, Hubbard (e.g., Hubbard and Bharucha, 1988) presented smooth stimulus motion and used motor responses. In contrast, Freyd (e.g., Freyd and Finke, 1984) presented implied stimulus motion and used the method of constant stimuli. The same forward error was observed in both paradigms. However, the processes underlying the error may be very different. When smooth stimulus motion is followed by smooth pursuit eye movements, the forward error is associated with asynchronous processing of retinal and extraretinal information. In the absence of eye movements, no forward displacement is observed with smooth motion. In contrast, implied motion produces a forward error even without eye movements, suggesting that observers extrapolate the next target step when successive target presentations are far apart. Finally, motor responses produce errors that are not observed with perceptual judgments, indicating that the motor system may compensate for neuronal latencies.     

Comment and Reply Why eye movements and perceptual factors have to be controlled in studies on “representational momentum”

In order to study memory of the final position of a smoothly moving target, Hubbard (e.g., Hubbard & Bharucha, 1988) presented smooth stimulus motion and used motor responses. In contrast, Freyd (e.g., Freyd & Finke, 1984) presented implied stimulus motion and used the method of constant stimuli. The same forward error was observed in both paradigms. However, the processes underlying the error may be very different. When smooth stimulus motion is followed by smooth pursuit eye movements, the forward error is associated with asynchronous processing of retinal and extraretinal information. In the absence of eye movements, no forward displacement is observed with smooth motion. In contrast, implied motion produces a forward error even without eye movements, suggesting that observers extrapolate the next target step when successive target presentations are far apart. Finally, motor responses produce errors that are not observed with perceptual judgments, indicating that the motor system may compensate for neuronal latencies.     

Illusory motion induced by blurred red-blue edges

Visual patterns consisting of a red-and-blue region with a blurry edge yield illusory motion. Eye movements over a static pattern induced illusory motion of the edge in the direction opposite to the eye movement. The illusion also takes place for patterns in motion without eye movement. The illusion suggests the effect of colour combination on the spatial perception of a blurry edge.     

Extraretinal and retinal amplitude and phase errors during Filehne illusion and path perception

Pursuit eye movements give rise to retinal motion. To judge stimulus motion relative to the head, the visual system must correct for the eye movement by using an extraretinal, eye-velocity signal. Such correction is important in a variety of motion estimation tasks including judgments of object motion relative to the head and judgments of self-motion direction from optic flow. The Filehne illusion (where a stationary object appears to move opposite to the pursuit) results from a mismatch between retinal and extraretinal speed estimates. A mismatch in timing could also exist. Speed and timing errors were investigated using sinusoidal pursuit eye movements. We describe a new illusion--the slalom illusion--in which the perceived direction of self-motion oscillates left and right when the eyes move sinusoidally. A linear model is presented that determines the gain ratio and phase difference of extraretinal and retinal signals accompanying the Filehne and slalom illusions. The speed mismatch and timing differences were measured in the Filehne and self-motion situations using a motion-nulling procedure. Timing errors were very small for the Filehne and slalom illusions. However, the ratios of extraretinal to retinal gain were consistently less than 1, so both illusions are the consequence of a mismatch between estimates of retinal and extraretinal speed. The relevance of the results for recovering the direction of self-motion during pursuit eye movements is discussed.     

Centripetal force draws the eyes,not memory of the target,toward the center

Many observers believe that a target will continue on a curved trajectory after exiting a spiral tube. Similarly, when observers were asked to localize the final position of a target moving on a circular orbit, displacement of the judged position in the direction of forward motion ("representational momentum") and toward the center of the orbit was observed (cf. T. L. Hubbard, 1996). The present study shows that memory displacement of targets on a circular orbit is affected by eye movements. Forward displacement was larger with ocular pursuit of the target, whereas inward displacement was larger with motionless eyes. The results challenge an account attributing forward and inward displacement to mental analogues of momentum and centripetal force, respectively.     

Induced motion of a fixated target: influence of voluntary eye deviation.

Induced motion (IM) was observed in a fixated target in the direction opposite to the real motion of a moving background. Relative to a fixation target located straight ahead, IM decreased when fixation was deviated 10 degrees in the same direction as background motion and increased when fixation was deviated 10 degrees opposite background motion. These results are consistent with a "nystagmus-suppression" hypothesis for subjective motion of fixated targets: the magnitude of illusory motion is correlated with the amount of voluntary efference required to oppose involuntary eye movements that would occur in the absence of fixation. In addition to the form of IM studied, this explanation applies to autokinesis, apparent concomitant motion, and the oculogyral illusion. Accounts of IM that stress visual capture of vection, afferent mechanisms, egocenter deviations, or phenomenological principles, although they may explain some forms of IM, do not account for the present results.     

Additivity of retinal and pursuit velocity in the perceptions of depth and rigidity from object-produced motion parallax

Two psychophysical experiments were conducted to investigate the mechanism that generates stable depth structure from retinal motion combined with extraretinal signals from pursuit eye movements. Stimuli consisted of random dots that moved horizontally in one direction (ie stimuli had common motion on the retina), but at different speeds between adjacent rows. The stimuli were presented with different speeds of pursuit eye movements whose direction was opposite to that of the common retinal motion. Experiment 1 showed that the rows moving faster on the retina appeared closer when viewed without eye movements; however, they appeared farther when pursuit speed exceeded the speed of common retinal motion. The 'transition' speed of the pursuit eye movement was slightly, but consistently, larger than the speed of common retinal motion. Experiment 2 showed that parallax thresholds for perceiving relative motion between adjacent rows were minimum at the transition speed found in experiment 1. These results suggest that the visual system calculates head-centric velocity, by adding retinal velocity and pursuit velocity, to obtain a stable depth structure.     

The neural basis of smooth pursuit eye movements in the rhesus monkey brain

Smooth pursuit eye movements are performed in order to prevent retinal image blur of a moving object. Rhesus monkeys are able to perform smooth pursuit eye movements quite similar as humans, even if the pursuit target does not consist in a simple moving dot. Therefore, the study of the neuronal responses as well as the consequences of micro-stimulation and lesions in trained monkeys performing smooth pursuit is a powerful approach to understand the human pursuit system. The processing of visual motion is achieved in the primary visual cortex and the middle temporal area. Further processing including the combination of retinal image motion signals with extra-retinal signals such as the ongoing eye and head movement occurs in subsequent cortical areas as the medial superior temporal area, the ventral intraparietal area and the frontal and supplementary eye field. The frontal eye field especially contributes anticipatory signals which have a substantial influence on the execution of smooth pursuit. All these cortical areas send information to the pontine nuclei, which in turn provide the input to the cerebellum. The cerebellum contains two pursuit representations: in the paraflocculus/flocculus region and in the posterior vermis. While the first representation is most likely involved in the coordination of pursuit and the vestibular-ocular reflex, the latter is involved in the precise adjustments of the eye movements such as adaptation of pursuit initiation. The output of the cerebellum is directed to the moto-neurons of the extra-ocular muscles in the brainstem.     

Induced motion of a fixated target: Influence of voluntary eye deviation

Induced motion (IM) was observed in a fixated target in the direction opposite to the real motion of a moving background. Relative to a fixation target located straight ahead, IM decreased when fixation was deviated 10° in the same direction as background motion and increased when fixation was deviated 10° opposite background motion. These results are consistent with a “nystagmus-suppression” hypothesis for subjective motion of fixated targets: the magnitude of illusory motion is correlated with the amount of voluntary efference required to oppose involuntary eye movements that would occur in the absence of fixation. In addition to the form of IM studied, this explanation applies to autokinesis, apparent concomitant motion, and the oculogyral illusion. Accounts of IM that stress visual capture of vection, afferent mechanisms, egocenter deviations, or phenomenological principles, although they may explain some forms of IM, do not account for the present results.     

Retinal and extraretinal information in movement perception: how to invert the Filehne illusion

During a pursuit eye movement made in darkness across a small stationary stimulus, the stimulus is perceived as moving in the opposite direction to the eyes. This so-called Filehne illusion is usually explained by assuming that during pursuit eye movements the extraretinal signal (which informs the visual system about eye velocity so that retinal image motion can be interpreted) falls short. A study is reported in which the concept of an extraretinal signal is replaced by the concept of a reference signal, which serves to inform the visual system about the velocity of the retinae in space. Reference signals are evoked in response to eye movements, but also in response to any stimulation that may yield a sensation of self-motion, because during self-motion the retinae also move in space. Optokinetic stimulation should therefore affect reference signal size. To test this prediction the Filehne illusion was investigated with stimuli of different optokinetic potentials. As predicted, with briefly presented stimuli (no optokinetic potential) the usual illusion always occurred. With longer stimulus presentation times the magnitude of the illusion was reduced when the spatial frequency of the stimulus was reduced (increased optokinetic potential). At very low spatial frequencies (strongest optokinetic potential) the illusion was inverted. The significance of the conclusion, that reference signal size increases with increasing optokinetic stimulus potential, is discussed. It appears to explain many visual illusions, such as the movement aftereffect and center-surround induced motion, and it may bridge the gap between direct Gibsonian and indirect inferential theories of motion perception.     

The binocular representation of uniform motion

In the model of motion perception proposed by Swanston, Wade, and Day (1987, Perception 16 143-159) it was suggested that retinocentric motion and eye movement information are combined independently for each eye, to give left and right orbitocentric representations of movement. The weighted orbitocentric values are then added, to give a single agocentric representation. It is shown that for a physical motion observed without pursuit eye movements this formulation predicts a reduction in the perceived extent of motion with monocular as opposed to binocular viewing. This prediction was tested, and shown to be incorrect. Accordingly, a modification of the model is proposed, in which the left and right retinocentric signals are weighted according to the presence or absence of stimulation, and combined to give a binocular retinocentric representation. In a similar way left-eye and right-eye position signals are combined to give a single binocular eye movement signal for version. This is then added to the binocular retinocentric signal to give the egocentric representation. This modification provides a unified account of both static visual direction and movement perception.     

Kinematic property of target motion conditions gaze behavior and eye-hand synergy during manual tracking

This study investigated how frequency demand and motion feedback influenced composite ocular movements and eye-hand synergy during manual tracking. Fourteen volunteers conducted slow and fast force-tracking in which targets were displayed in either line-mode or wave-mode to guide manual tracking with target movement of direct position or velocity nature. The results showed that eye-hand synergy was a selective response of spatiotemporal coupling conditional on target rate and feedback mode. Slow and line-mode tracking exhibited stronger eye-hand coupling than fast and wave-mode tracking. Both eye movement and manual action led the target signal during fast-tracking, while the latency of ocular navigation during slow-tracking depended on the feedback mode. Slow-tracking resulted in more saccadic responses and larger pursuit gains than fast-tracking. Line-mode tracking led to larger pursuit gains but fewer and shorter gaze fixations than wave-mode tracking. During slow-tracking, incidences of saccade and gaze fixation fluctuated across a target cycle, peaking at velocity maximum and the maximal curvature of target displacement, respectively. For line-mode tracking, the incidence of smooth pursuit was phase-dependent, peaking at velocity maximum as well. Manual behavior of slow or line-mode tracking was better predicted by composite eye movements than that of fast or wave-mode tracking. In conclusion, manual tracking relied on versatile visual strategies to perceive target movements of different kinematic properties, which suggested a flexible coordinative control for the ocular and manual sensorimotor systems.     

Attention maintains mental extrapolation of target position: irrelevant distractors eliminate forward displacement after implied motion

Observers' judgments of the final position of a moving target are typically shifted in the direction of implied motion ("representational momentum"). The role of attention is unclear: visual attention may be necessary to maintain or halt target displacement. When attention was captured by irrelevant distractors presented during the retention interval, forward displacement after implied target motion disappeared, suggesting that attention may be necessary to maintain mental extrapolation of target motion. In a further corroborative experiment, the deployment of attention was measured after a sequence of implied motion, and faster responses were observed to stimuli appearing in the direction of motion. Thus, attention may guide the mental extrapolation of target motion. Additionally, eye movements were measured during stimulus presentation and retention interval. The results showed that forward displacement with implied motion does not depend on eye movements. Differences between implied and smooth motion are discussed with respect to recent neurophysiological findings.     

Visual stimulation affects the perception of voluntary leg movements during walking

When a limb is used for locomotion, patterns of afferent and efferent activity related to its own motion are present as well as visual, vestibular, and other proprioceptive information about motion of the whole body. A study is reported in which it was asked whether visual stimulation present during whole-body motion can influence the perception of the leg movements propelling the body. Subjects were tested in conditions in which the stepping movements they made were identical but the amount of body displacement relative to inertial space and to the visual surround varied. These test conditions were created by getting the subjects to walk on a rotatable platform centered inside a large, independently rotatable, optokinetic drum. In each test condition, subjects, without looking at their legs, compared, against a standard condition in which the floor and drum were both stationary, their speed of body motion, their stride length and stepping rate, the direction of their steps, and the perceived force they exerted during stepping. When visual surround motion was incompatible with the motion normally associated with the stepping movements being made, changes in apparent body motion and in the awareness of the frequency, extent, and direction of the voluntary stepping movements resulted.     

Gaze stability of observers watching Op Art pictures

It has been the matter of some debate why we can experience vivid dynamic illusions when looking at static pictures composed from simple black and white patterns. The impression of illusory motion is particularly strong when viewing some of the works of 'Op Artists, such as Bridget Riley's painting Fall. Explanations of the illusory motion have ranged from retinal to cortical mechanisms, and an important role has been attributed to eye movements. To assess the possible contribution of eye movements to the illusory-motion percept we studied the strength of the illusion under different viewing conditions, and analysed the gaze stability of observers viewing the Riley painting and control patterns that do not produce the illusion. Whereas the illusion was reduced, but not abolished, when watching the painting through a pinhole, which reduces the effects of accommodation, it was not perceived in flash afterimages, suggesting an important role for eye movements in generating the illusion for this image. Recordings of eye movements revealed an abundance of small involuntary saccades when looking at the Riley pattern, despite the fact that gaze was kept within the dedicated fixation region. The frequency and particular characteristics of these rapid eye movements can vary considerably between different observers, but, although there was a tendency for gaze stability to deteriorate while viewing a Riley painting, there was no significant difference in saccade frequency between the stimulus and control patterns. Theoretical considerations indicate that such small image displacements can generate patterns of motion signals in a motion-detector network, which may serve as a simple and sufficient, but not necessarily exclusive, explanation for the illusion. Why such image displacements lead to perceptual results with a group of Op Art and similar patterns, but remain invisible for other stimuli, is discussed.     

The effect of prolonged practice of pursuit eye movement

Prolonged exposure to a reciprocating motion that is tracked by the eyes results in diminished extent of perceived motion. Investigation of this effect showed that it becomes manifest only in perceived motion that is caused by ocular pursuit, but that it is not an eye muscle effect. It may consist in a changed evaluation of eye movements. The results throw some light on the relations between the processes that are caused by different stimuli for motion.