Does cortical motion adaptation exhibit functional properties analogous to light adaptation in the retina?

PURPOSE: The retina codes variations in luminance by adapting to and hence discounting, the mean luminance. During adaptation to a moving pattern, perceived speed decreases. Thus we know that the adapted visual system does not simply code the absolute speed of a stimulus. We hypothesize that adaptation to a moving stimulus serves to optimize coding of changes in speed at the expense of maintaining an accurate representation of absolute speed. In this case we would expect discrimination of speeds around the adapted level to be preserved or enhanced by motion adaptation. METHODS AND RESULTS: After adaptation to motion in the same direction as a subsequent test stimulus, seven of eight subjects showed a reduction of perceived speed in the adapted region and seven showed enhanced discrimination. CONCLUSIONS: We conclude that motion adaptation preserves or enhances differential speed sensitivity at the expense of an accurate representation of absolute speed in a manner analogous to retinal light adaptation.     

The direction aftereffect is driven by adaptation of local motion detectors

The processing of motion information by the visual system can be decomposed into two general stages; point-by-point local motion extraction, followed by global motion extraction through the pooling of the local motion signals. The direction aftereffect (DAE) is a well known phenomenon in which prior adaptation to a unidirectional moving pattern results in an exaggerated perceived direction difference between the adapted direction and a subsequently viewed stimulus moving in a different direction. The experiments in this paper sought to identify where the adaptation underlying the DAE occurs within the motion processing hierarchy. We found that the DAE exhibits interocular transfer, thus demonstrating that the underlying adapted neural mechanisms are binocularly driven and must, therefore, reside in the visual cortex. The remaining experiments measured the speed tuning of the DAE, and used the derived function to test a number of local and global models of the phenomenon. Our data provide compelling evidence that the DAE is driven by the adaptation of motion-sensitive neurons at the local-processing stage of motion encoding. This is in contrast to earlier research showing that direction repulsion, which can be viewed as a simultaneous presentation counterpart to the DAE, is a global motion process. This leads us to conclude that the DAE and direction repulsion reflect interactions between motion-sensitive neural mechanisms at different levels of the motion-processing hierarchy.     

Adaptation to one perceived motion direction can generate multiple velocity aftereffects

Sensory adaptation is a useful tool to identify the links between perceptual effects and neural mechanisms. Even though motion adaptation is one of the earliest and most documented aftereffects, few studies have investigated the perception of direction and speed of the aftereffect at the same time, that is the perceived velocity. Using a novel experimental paradigm, we simultaneously recorded the perceived direction and speed of leftward or rightward moving random dots before and after adaptation. For the adapting stimulus, we chose a horizontally-oriented broadband grating moving upward behind a circular aperture. Because of the aperture problem, the interpretation of this stimulus is ambiguous, being consistent with multiple velocities, and yet it is systematically perceived as moving at a single direction and speed. Here we ask whether the visual system adapts to the multiple velocities of the adaptor or to just the single perceived velocity. Our results show a strong repulsion aftereffect, away from the adapting velocity (downward and slower), that increases gradually for faster test stimuli as long as these stimuli include some velocities that match some of the ambiguous ones of the adaptor. In summary, the visual system seems to adapt to the multiple velocities of an ambiguous stimulus even though a single velocity is perceived. Our findings can be well described by a computational model that assumes a joint encoding of direction and speed and that includes an extended adaptation component that can represent all the possible velocities of the ambiguous stimulus.     

Local velocity representation: evidence from motion adaptation

Adaptation to a moving visual pattern induces shifts in the perceived motion of subsequently viewed moving patterns. Explanations of such effects are typically based on adaptation-induced sensitivity changes in spatio-temporal frequency tuned mechanisms (STFMs). An alternative hypothesis is that adaptation occurs in mechanisms that independently encode direction and speed (DSMs). Yet a third possibility is that adaptation occurs in mechanisms that encode 2D pattern velocity (VMs). We performed a series of psychophysical experiments to examine predictions made by each of the three hypotheses. The results indicate that: (1) adaptation-induced shifts are relatively independent of spatial pattern of both adapting and test stimuli; (2) the shift in perceived direction of motion of a plaid stimulus after adaptation to a grating indicates a shift in the motion of the plaid pattern, and not a shift in the motion of the plaid components; and (3) the 2D pattern of shift in perceived velocity radiates away from the adaptation velocity, and is inseparable in speed and direction of motion. Taken together, these results are most consistent with the VM adaptation hypothesis.     

Test stimulus characteristics determine the perceived speed of the dynamic motion aftereffect

Using a speed-matching task, we measured the speed tuning of the dynamic motion aftereffect (MAE). The results of our first experiment, in which we co-varied dot speed in the adaptation and test stimuli, revealed a speed tuning function. We sought to tease apart what contribution, if any, the test stimulus makes towards the observed speed tuning. This was examined by independently manipulating dot speed in the adaptation and test stimuli, and measuring the effect this had on the perceived speed of the dynamic MAE. The results revealed that the speed tuning of the dynamic MAE is determined, not by the speed of the adaptation stimulus, but by the local motion characteristics of the dynamic test stimulus. The role of the test stimulus in determining the perceived speed of the dynamic MAE was confirmed by showing that, if one uses a test stimulus containing two sources of local speed information, observers report seeing a transparent MAE; this is despite the fact that adaptation is induced using a single-speed stimulus. Thus while the adaptation stimulus necessarily determines perceived direction of the dynamic MAE, its perceived speed is determined by the test stimulus. This dissociation of speed and direction supports the notion that the processing of these two visual attributes may be partially independent.     

Perceptual manifestations of fast neural plasticity: motion priming, rapid motion aftereffect and perceptual sensitization

Visual neurons show fast adaptive behavior in response to brief visual input. However, the perceptual consequences of this rapid neural adaptation are less known. Here, we show that brief exposure to a moving adaptation stimulus-ranging from tens to hundreds of milliseconds-influences the perception of a subsequently presented ambiguous motion test stimulus. Whether the ambiguous motion is perceived to move in the same direction (priming), or in the opposite direction (rapid motion aftereffect) varies systematically with the duration of the adaptation stimulus and the adaptation-test blank interval. These biases appear and decay rapidly. Moreover, when the adapting stimulus is itself ambiguous, these effects are not produced. Instead, the percept for the subsequent test stimulus is biased to the perceived direction of the adaptation stimulus. This effect (perceptual sensitization) builds gradually over the time between the adaptation and test stimuli. Our results indicate that rapid adaptation plays a role mainly within early motion processing, whereas a slow potentiation controls the sensitivity at a later stage.     

Direction-specific adaptation of magnetic responses to motion onset

We investigated the direction-specificity of motion adaptation, by recording magnetic responses evoked by motion onsets under both adapted and control conditions. The inter-stimulus interval was equated between the conditions to precisely evaluate the effect of motion adaptation itself. The onset stimuli at 1.5, 3.0 or 6.0 deg/s moved in the same direction or in the opposite direction to an adaptation stimulus at 3.0 deg/s. The perceived velocity of each test stimulus was measured in separate sessions. The most prominent peak (M2) of evoked responses appeared around 200-300 ms after motion onsets, and the dipoles were mainly estimated in the temporo-occipital area. Adaptation largely affected both perceived velocities and the M2 amplitudes. The M2 amplitudes were decreased by adaptation for both directions of test stimuli, and the decreases were significantly larger for the test stimuli in the adapted direction (49-63% of control condition) than for the test stimuli in the opposite direction (17-27% of control condition). The present study, for the first time, found that magnetic responses evoked by motion onsets reflect the activities of neurons that have direction-specificity.     

Nulling the motion aftereffect with dynamic random-dot stimuli: limitations and implications

We used biased random-dot dynamic test stimuli to measure the strength of the motion aftereffect (MAE) to evaluate the usefulness of this technique as a measure of motion adaptation strength. The stimuli consisted of noise dots whose individual directions were random and of signal dots moving in a unique direction. All dots moved at the same speed. For each condition, the nulling percentage (percentage of signal dots needed to perceptually null the MAE) was scaled with respect to the coherence threshold (percentage needed to perceive the coherent motion of signal dots without prior adaptation). The increase of these scaled values with the density of dots in the test stimulus suggests that MAE strength is underestimated when measured with low densities. We show that previous reports of high nulling percentages at slow speeds do not reflect strong MAEs, but are actually due to spatio-temporal aliasing, which dramatically increases coherence thresholds. We further show that MAE strength at slow speed increases with eccentricity. These findings are consistent with the idea that using this dynamic test stimulus preferentially reveals the adaptation of a population of high-speed motion units whose activity is independent of adapted low-speed motion units.     

Visual motion detection sensitivity is enhanced by an orthogonal motion aftereffect

A recent study (H. Takemura & I. Murakami, 2010) showed enhancement of motion detection sensitivity by an orthogonal induced motion, suggesting that a weak motion component can combine with an orthogonal motion component to generate stronger oblique motion perception. Here we examined how an orthogonal motion aftereffect (MAE) affects motion detection sensitivity. After adaptation to vertical motion, a Gabor patch barely moving leftward or rightward was presented. As a result of an interaction between horizontal physical motion and a vertical MAE, subjects perceived the stimulus as moving obliquely. Subjects were asked to judge the horizontal direction of motion irrespective of the vertical MAE. The performance was enhanced when the Gabor patch was perceived as moving obliquely as the result of a weak MAE. The enhancement effect depended on the strength of the MAE for each subject rather than on the temporal frequency of the adapting stimulus. These results suggest that weak motion information that is hard to detect can interact with orthogonal adaptation and yield stronger oblique motion perception, making directional judgment easier. Moreover, the present results indicate that the enhancement effect of orthogonal motion involves general motion integration mechanisms rather than a specific mechanism only applicable to a particular type of illusory motion.     

Center-surround effects on perceived speed

We investigated whether center-surround interactions affect perceived speed in a manner similar to their effects on direction discrimination thresholds [e.g. Tadin, D., Lappin, J. S., Gilroy, L. A., & Blake, R. (2003). Perceptual consequences of center-surround antagonism in visual motion processing. Nature, 424, 312-315]. Observers were asked to match the speed of a test stimulus (a grating, with fixed contrast and no surround) to that of a reference stimulus of variable contrast and with a variably sized surround, moving at one of two possible velocities (1 and 12 cps). At 1-cps, both lowering contrast and increasing surround-size resulted in a decrease in perceived speed, except for very low contrast stimuli, where a larger surround resulted in an increase in perceived speed. Although the effect of surround-size was comparable in the two velocity conditions, the effect of contrast was different at 12-cps. That is, in the 12 cps condition, a decrease in perceived speed was observed only for the lowest contrast used. Our results suggest that, at least for the lower velocity used, center-surround interactions affect perceived speed in a manner analogous to their effect on direction discrimination.     

Evidence for a subtractive component in motion adaptation

Adaptation to a moving stimulus changes the perception of a stationary grating and also reduces contrast sensitivity to the adaptor. We determined whether the first effect could be predicted from the second. The contrast discrimination (T vs. C) function for a drifting 7.5 Hz grating test stimulus was determined when observers were adapted to a low contrast (0.075) grating of the same spatial and temporal frequency, moving in either the same or the opposite direction as the test. The effect of an adaptor moving in the same direction was to move the T vs. C function upwards and to the right, in a manner consistent with an increase in divisive inhibition. We also measured the effect of adaptation on the motion-null point for a counterphasing grating containing two components, one moving in the same direction as the adaptor and the other in the opposite direction. Adaptation increased the amount of contrast of the adapted component required to achieve the motion-null point. However, this shift could not be predicted from the effects of adaptation on contrast sensitivity. In particular, the balance point was shifted in gratings of high contrast where there was no effect of adaptation on contrast discrimination. We suggest that adaptation has a subtractive (recalibration) effect in addition to its effects on the contrast transduction function, and that this subtractive effect may explain the movement after-effect seen with stationary tests.     

Human discrimination of visual direction of motion with and without smooth pursuit eye movements

It has long been known that ocular pursuit of a moving target has a major influence on its perceived speed (Aubert, 1886; Fleischl, 1882). However, little is known about the effect of smooth pursuit on the perception of target direction. Here we compare the precision of human visual-direction judgments under two oculomotor conditions (pursuit vs. fixation). We also examine the impact of stimulus duration (200 ms vs. ~800 ms) and absolute direction (cardinal vs. oblique). Our main finding is that direction discrimination thresholds in the fixation and pursuit conditions are indistinguishable. Furthermore, the two oculomotor conditions showed oblique effects of similar magnitudes. These data suggest that the neural direction signals supporting perception are the same with or without pursuit, despite remarkably different retinal stimulation. During fixation, the stimulus information is restricted to large, purely peripheral retinal motion, while during steady-state pursuit, the stimulus information consists of small, unreliable foveal retinal motion and a large efference-copy signal. A parsimonious explanation of our findings is that the signal limiting the precision of direction judgments is a neural estimate of target motion in head-centered (or world-centered) coordinates (i.e., a combined retinal and eye motion signal) as found in the medial superior temporal area (MST), and not simply an estimate of retinal motion as found in the middle temporal area (MT).     

A motion aftereffect seen more strongly by the non-adapted eye: evidence of multistage adaptation in visual motion processing

We found that the motion aftereffect measured using a directionally ambiguous counterphase grating (flicker MAE) can be stronger when it is measured for the non-adapted eye than when measured for the adapted eye. The monocularly viewed adaptation stimulus was the movement of a missing-fundamental grating (2f+3f motion), for which the movement of the higher-order spatial structure was dominantly perceived, while the first-order structure was physically moving in the opposite direction. For observers who perceived the MAE consistently in the direction opposite to the movement of the higher-order structures, the MAE was larger for the non-adapted eye than for the adapted eye. This finding of 'over-100% transfer' invalidates the standard view that the IOT is a direct measure of the binocularity of the adapted neurones. In addition, the finding provides convincing support for the hypothesis that the flicker MAE reflects adaptation at multiple processing stages     

Eye movements affect the perceived speed of visual motion.

Eye movements add a constant displacement to the visual scene, altering the retinal-image velocity. Therefore, in order to recover the real world motion, eye-movement effects must be compensated. If full compensation occurs, the perceived speed of a moving object should be the same regardless of whether the eye is stationary or moving. Using a pursue-fixate procedure in a perceptual matching paradigm, we found that eye movements systematically bias the perceived speed of the distal stimulus, indicating a lack of compensation. Speed judgments depended on the interaction between the distal stimulus size and the eye velocity relative to the distal stimulus motion. When the eyes and distal stimulus moved in the same direction, speed judgments of the distal stimulus approximately matched its retinal-image motion. When the eyes and distal stimulus moved in the opposite direction, speed judgments depended on the stimulus size. For small sizes, perceived speed was typically overestimated. For large sizes, perceived speed was underestimated. Results are explained in terms of retinal-extraretinal interactions and correlate with recent neurophysiological findings.     

Effect of signal intensity on perceived speed

The effect of signal intensity (proportion of dots moving in the same direction compared to noise dots that move in random directions) on perceived speed was investigated. It was found that increasing signal level decreased the perceived speed of the stimulus. This finding indicates that global-motion pooling processes play a role in the extraction of speed information. It is suggested that the amount of relative motion in the stimulus influences perceived speed, with perceived speed increasing with increasing relative motion. The results are discussed in relation to the notion that speed and direction are processed, at least in part, differently.     

Independent coding of object motion and position revealed by distinct contingent aftereffects

Despite several findings of perceptual asynchronies between object features, it remains unclear whether independent neuronal populations necessarily code these perceptually unbound properties. To examine this, we investigated the binding between an object's spatial frequency and its rotational motion using contingent motion aftereffects (MAE). Subjects adapted to an oscillating grating whose direction of rotation was paired with a high or low spatial frequency pattern. In separate adaptation conditions, we varied the moment when the spatial frequency change occurred relative to the direction reversal. After adapting to one stimulus, subjects made judgments of either the perceived MAE (rotational movement) or the position shift (instantaneous phase rotation) that accompanied the MAE. To null the spatial frequency-contingent MAE, motion reversals had to physically lag changes in spatial frequency during adaptation. To null the position shift that accompanied the MAE, however, no temporal lag between the attributes was required. This demonstrates that perceived motion and position can be perceptually misbound. Indeed, in certain conditions, subjects perceived the test pattern to drift in one direction while its position appeared shifted in the opposite direction. The dissociation between perceived motion and position of the same test pattern, following identical adaptation, demonstrates that distinguishable neural populations code for these object properties.     

Wohlgemuth was right: distracting attention from the adapting stimulus does not decrease the motion after-effect

We determined whether distracting the observer’s attention from an adapting stimulus could decrease the motion after-effect. Unlike previous studies we used a relatively bias-free 2AFC procedure to measure the strength of adaptation. The strength of motion adaptation was measured by the effects of a moving grating on the contrast discrimination (T vs. C) function for gratings moving in the same or opposite direction. As in previous reports, the effect of adaptation was to move the T vs. C function upwards and rightwards, consistent with an increase in the C50 (semi-saturation) response in the transduction function of the neural mechanism underlying the discrimination. On the other hand, manipulating the attentional load of a distracting task during adaptation had no consistent effect on contrast discrimination, including the absolute detection threshold. It is suggested that previous reported effects of attentional load on adaptation may have depended on response bias, rather than changes in sensitivity.     

An effect of relative motion on trajectory discrimination

Psychophysical studies point to the existence of specialized mechanisms sensitive to the relative motion between an object and its background. Such mechanisms would seem ideal for the motion-based segmentation of objects; however, their properties and role in processing the visual scene remain unclear. Here we examine the contribution of relative motion mechanisms to the processing of object trajectory. In a series of four psychophysical experiments we examine systematically the effects of relative direction and speed differences on the perceived trajectory of an object against a moving background. We show that background motion systematically influences the discrimination of object direction. Subjects' ability to discriminate direction was consistently better for objects moving opposite a translating background than for objects moving in the same direction as the background. This effect was limited to the case of a translating background and did not affect perceived trajectory for more complex background motions associated with self-motion. We interpret these differences as providing support for the role of relative motion mechanisms in the segmentation and representation of object motions that do not occlude the path of an observer's self-motion.     

Reduction in the motion coherence threshold for the same direction as that perceived during adaptation

When a stimulus of equally spaced parallel lines is displaced slightly in a direction perpendicular to the lines, low-speed motion toward the displacement direction can be perceived. Such a stimulus embodies both a low-speed and a high-speed component in opposite directions. The dominance of the former would result in the perception of low-speed motion. To see how the unperceived high-speed component is processed by the visual system, I measured coherence thresholds for random-dot test-motion with and without prior adaptation to the low-speed motion of the equally spaced parallel lines. The results depended on the test speeds. At low speeds, the coherence thresholds for the same direction as that perceived during the adaptation phase increased and the coherence thresholds for the opposite direction decreased. At high speeds, the same adaptation resulted in an opposite effect. The threshold reduction for high-speed motion in the same direction as that perceived during the adaptation phase and the threshold elevation in the opposite direction might be due to adaptation of a high-speed processing channel to the high-speed component that was not perceived but was nevertheless detected.     

Perceiving motion transparency in the absence of component direction differences

The simultaneous perception of multiple motion components within the same region in the visual field is a difficult processing task, which can be solved by human observers for a range of transparently moving stimuli. We use transparently moving gratings to study this phenomenon psychophysically, focussing on configurations in which individual components move in the same direction and can only be discriminated by speed differences. We first demonstrate that the stimuli are perceived as transparent and then proceed to quantify how the strength of motion transparency changes while component grating parameters such as fundamental spatial frequency, speed and luminance are varied. The results were consistent with perception resolving a signal detection task of separating two superimposed global motion signals corresponding to each of the components. We also identify the importance of broadband stimuli containing edges, both for perceiving transparency with the same direction stimulus configuration, and for static transparency. The local density of edges has a direct influence on the strength of perceived transparency, suggesting that local motion detection at the edges of the stimuli, which is sensitive to speed differences, may be critical to solve the task. The work suggests that there may be a simultaneous retinotopic representation of the two speeds of motion analogous to that accomplished by the motion direction tuned neurons found across regions of visual cortex.