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.     

Common and independent processing of visual motion perception and oculomotor response

Visual motion signals are used not only to drive motion perception but also to elicit oculomotor responses. A fundamental question is whether perceptual and oculomotor processing of motion signals shares a common mechanism. This study aimed to address this question using visual motion priming, in which the perceived direction of a directionally ambiguous stimulus is biased in the same (positive priming) or opposite (negative priming) direction as that of a priming stimulus. The priming effect depends on the duration of the priming stimulus. It is assumed that positive and negative priming are mediated by high- and low-level motion systems, respectively. Participants were asked to judge the perceived direction of a π-phase-shifted test grating after a smoothly drifting priming grating during varied durations. Their eye movements were measured while the test grating was presented. The perception and eye movements were discrepant under positive priming and correlated under negative priming on a trial-by-trial basis when an interstimulus interval was inserted between the priming and test stimuli, indicating that the eye movements were evoked by the test stimulus per se. These findings suggest that perceptual and oculomotor responses are induced by a common mechanism at a low level of motion processing but by independent mechanisms at a high level of motion processing.     

Preexposure disrupts learning of location-contingent perceptual biases for ambiguous stimuli

The perception of a bistable stimulus as one or the other interpretation can be biased by prior presentations of that stimulus. Such learning effects have been found to be long lasting even after small amounts of training. The effectiveness of training may be influenced by preexposure to the ambiguous stimulus. Here we investigate the role of preexposure for learning a position-dependent perceptual bias. We used rotating Necker Cubes as the bistable stimuli, which were presented at two locations: above or below fixation. On training trials, additional depth cues disambiguated the rotation direction contingent on the location. On test trials, the rotating cube was presented without disambiguation cues. Without preexposure to the ambiguous stimulus, subjects learned to perceive the cube to be rotating in the trained direction for both locations. However, subjects that were preexposed to the ambiguous stimulus did not learn the trained percept-location contingency, even though the preexposure was very short compared to the subsequent training. Preexposure to the disambiguated stimulus did not interfere with learning. This indicates a fundamental difference between ambiguous test and disambiguated training trials for learning a perceptual bias. In short, small variations in paradigm can have huge effects for the learning of perceptual biases for ambiguous stimuli.     

Shifting eye balance using monocularly directed attention in normal vision

In binocular vision, even without conscious awareness of eye of origin, attention can be selectively biased toward one eye by presenting a visual stimulus uniquely to that eye. Monocularly directed visual cues can bias perceptual dominance, as shown by studies using discrete measures of percept changes in continuous-flash suppression. Here, we use binocular rivalry to determine whether eye-based visual cues can modulate eye balance using continuous percept reporting. Using a dual-task versus single-task paradigm, we investigated whether the attentional load of these cues differentially modulates eye balance. Furthermore, both color-based and motion-based cue stimuli, non-overlaid and peripheral to the rivalry grating stimuli, were used to determine whether shifts in eye balance were stimulus specific. Aligned to cue stimulus onset, time series of percept reports were constructed and averaged across trials and participants. Specifically, for the monocular attention conditions, we found a significant shift in eye balance toward the cued eye and a significant difference in the time taken to switch from the dominating percept, regardless of whether the attention stimuli is color based or motion based. Although we did not find a significant main effect of attentional load, we found a significant interaction effect between the attentionally cued eye and attentional load on the shift in eye balance, indicating an influence of monocular attention on the shift in eye balance.     

The effect of retinal illuminance on visual motion priming

The perceived direction of a directionally ambiguous stimulus is influenced by the moving direction of a preceding priming stimulus. Previous studies have shown that a brief priming stimulus induces positive motion priming, in which a subsequent directionally ambiguous stimulus is perceived to move in the same direction as the primer, while a longer priming stimulus induces negative priming, in which the following ambiguous stimulus is perceived to move in the opposite direction of the primer. The purpose of this study was to elucidate the underlying mechanism of motion priming by examining how retinal illuminance and velocity of the primer influences the perception of priming. Subjects judged the perceived direction of 180-deg phase-shifted (thus directionally ambiguous) sine-wave gratings displayed immediately after the offset of a primer stimulus. We found that perception of motion priming was greatly modulated by the retinal illuminance and velocity of the primer. Under low retinal illuminance, positive priming nearly disappeared even when the effective luminance contrast was equated between different conditions. Positive priming was prominent when the velocity of the primer was low, while only negative priming was observed when the velocity was high. These results suggest that the positive motion priming is induced by a higher-order mechanism that tracks prominent features of the visual stimulus, while a directionally selective motion mechanism induces negative motion priming.     

Self-operated stimuli improve subsequent visual motion integration

Evidences of perceptual changes that accompany motor activity have been limited primarily to audition and somatosensation. Here we asked whether motor learning results in changes to visual motion perception. We designed a reaching task in which participants were trained to make movements along several directions, while the visual feedback was provided by an intrinsically ambiguous moving stimulus directly tied to hand motion. We find that training improves coherent motion perception and that changes in movement are correlated with perceptual changes. No perceptual changes are observed in passive training even when observers were provided with an explicit strategy to facilitate single motion perception. A Bayesian model suggests that movement training promotes the fine-tuning of the internal representation of stimulus geometry. These results emphasize the role of sensorimotor interaction in determining the persistent properties in space and time that define a percept.     

Perceptual bistability with counterphase gratings

Suprathreshold counterphase modulated gratings induce a bistable percept of drift or flicker. It is argued that these perceptual alternations might provide a new means for the investigation of directional selective mechanisms. The prevalance of either of the two perceptions has been studied as a function of the spatio-temporal characteristics of the stimulus and compared with: (1) the spatio-temporal contrast sensitivity surface for counterphase modulated gratings; (2) the motion/counterphase sensitivity ratio. Drift perception elicited by suprathreshold counterphase gratings attains a maximum for 8 c/deg, 12 Hz stimuli and decreases for any other experimental condition. For spatial frequencies below 1 c/deg, or temporal frequencies below 2 Hz, only flicker perception is reported. These phenomenal experiences do not show any systematic dependence on the involuntary eye movements of the observer. Comparison with the threshold measurements does not support their explanation in terms of the transient-sustained dichotomy, nor does it allow for a straightforward equivalance between the spatio-temporal characteristics of direction-selective mechanisms at threshold and at suprathreshold levels. It is suggested that the balance between flicker and motion is the perceptual outcome of the competition between lower and higher order motion detectors.     

The perceived motion of a stereokinetic stimulus

An ellipse rotating in the image plane can produce several different percepts. The two-dimensional (2D) percepts are either a rotating rigid ellipse or a constantly deforming non-rigid ellipse. The 3D percept is a rotating rigid circular disk that is tilted relative to the image plane. Stimuli that generate 3D percepts based on purely 2D rotational motion are known as stereokinetic stimuli. We examined the 3D percepts generated by the rotating ellipse stimulus. In theory, the motion of the 3D percept cannot be reliably inferred based on the 2D stimulus. When we quantitatively estimated observers' perceived motion, however, we found that the perceived motion was nearly identical across observers. These results suggest that all observers had similar 3D percepts. We assumed that given the 2D rotating ellipse stimulus the visual system generates a rigid 3D percept that is as slow and smooth as possible. The percepts predicted by these assumptions closely matched the experimental data. These findings suggest that perceptual ambiguity in stereokinetic stimuli is resolved using slow and smooth motion assumptions.     

Visual resolution of motion ambiguity with periodic luminance- and contrast-domain stimuli.

Visual motion processes were studied with luminance- and contrast-modulated gratings. A sine-wave luminance grating was displaced abruptly back and forth by 3/16 cycle. The display sequence is ambiguous in that each 3/16-cycle phase shift (short-path motion) could just as readily be seen as a 13/16-cycle shift (long-path motion) in the opposite direction. By varying the duration of the interval (IFI) between the two phase positions, the luminance of the IFI, or the spatial frequency of the grating, it was possible to bias the ambiguous percept in favor of short-path motions or long-path motions. A contrast-modulated grating displaced through 3/16 cycle always appeared t undergo short-path motion. Current motion models which incorporate Reichardt-type/energy mechanisms and certain types of auxiliary signal transformations which precede those mechanisms do not adequately explain the effects of IFI intensity on the perceived motion of a sinusoidal grating or the effect of IFI duration on the perceived motion of a contrast-modulated grating.     

Temporal dynamics of stereo correspondence bi-stability

Periodic stereoscopic stimuli offer multiple viable solutions to the stereo correspondence problem. When viewing such stimuli for prolonged periods of time, observers continually switch their perceptual state between alternative correspondence solutions. We examine the temporal dynamics of this correspondence bi-stability. Participants were presented with an ambiguous stereogram comprised of regularly spaced dots. This stimulus was perceived as a fronto-parallel plane situated either behind or in front of fixation, depending on the achieved correspondence solution. The stimulus was presented continuously for one minute, with participants instructed to report the sign of the perceived depth at the sound of an auditory prompt presented, on average, every 2 s. Inter-ocular contrast and available disparities were varied so as to manipulate preferred correspondence. We find that participants are initially biased to perceive the stimulus as having an uncrossed disparity. Furthermore, we find that following an initial period of change, perceptual preference and perceptual stability (measured as the probability of an observer's percept changing between consecutive responses) remain constant over the presentation period. Finally, we find that manipulations of matching preference affect both the transient preference for, and stability of, one percept over another. Our results suggest two distinct phases of biasing in the correspondence matching process, one early, the other sustained.     

Uninformative visual experience establishes long term perceptual bias

Visual appearance depends upon the resolution of ambiguities that arise when 2D retinal images are interpreted as 3D scenes. This resolution may be characterized as a form of Bayesian perceptual inference, whereby retinal sense data combine with prior belief to yield an interpretation. Under this framework, the prior reflects environmental statistics, so an efficient system should learn by changing its prior after exposure to new statistics. We conjectured that a prior would only be modified when sense data contain disambiguating information, such that it is clear what bias is appropriate. This conjecture was tested by using a perceptually bistable stimulus, a rotating wire-frame cube, as a sensitive indicator of changes in the prior for 3D rotation direction, and by carefully matching perceptual experience of ambiguous and unambiguous versions of the stimulus across three groups of observers. We show for the first time that changes in the prior—observed as a change in bias that resists reverse learning the next day—is affected more by ambiguous stimuli than by disambiguated stimuli. Thus, contrary to our conjecture, modification of the prior occurred preferentially when the observer actively resolved ambiguity rather than when the observer was exposed to environmental contingencies. We propose that resolving stimuli that are not easily interpreted by existing visual rules must be a valid method for establishing useful perceptual biases in the natural world.     

Ambiguity in the perception of moving stimuli is resolved in favour of the cardinal axes

The aim of this study was to determine whether there is a link between the statistical properties of natural scenes and our perception of moving surfaces. Accordingly, we devised an ambiguous moving stimulus that could be perceived as moving in one of three directions of motion. The stimulus was a circular patch containing three square-wave drifting gratings. One grating was always either horizontal or vertical; the other two had component directions of drift at 120 degrees to the first (and to each other), producing four possible stimulus geometries. These were presented in a pseudorandom sequence. In brief presentations, subjects always perceived two of the gratings to cohere and move as a pattern in one direction, and the third grating to move independently in the opposite direction (its component direction). Although there were three equally plausible axes (one cardinal and two oblique) along which the coherent and independent motions could occur, subjects routinely saw motion along one of the cardinal axes. Thus, the visual system preferentially combines the two oblique gratings to form a pattern that drifts in the opposite direction to the cardinal grating. It was only when the contrast of one of the oblique gratings was changed that an oblique axis of motion was perceived. This perceptual anisotropy can be related to naturally occurring bias in the visual environment, notably the predominance of horizontal and vertical contours in our visual world.     

The oblique plaid effect

Plaids are ambiguous stimuli that can be perceived either as a coherent pattern moving rigidly or as two gratings sliding over each other. Here we report a new factor that affects the relative strength of coherency versus transparency: the global direction of motion of the plaid. Plaids moving in oblique directions are perceived as sliding more frequently than plaids moving in cardinal directions. We term this the oblique plaid effect. There is also a difference between the two cardinal directions: for most observers, plaids moving in horizontal directions cohere more than plaids moving in vertical directions. Two measures were used to quantify the relative strength of coherency vs. transparency: C/[C+T] and RTtransp. Those measures were derived from dynamics data obtained in long-duration trials (>1 min) where observers continually indicated their percept. The perception of plaids is bi-stable: over time it alternates between coherency and transparency, and the dynamics data reveal the relative strength of the two interpretations [Vision Research 43 (2003) 531]. C/[C+T] is the relative cumulative time spent perceiving coherency; RTtransp is the time between stimulus onset and the first report of transparency. The dynamics-based measures quantify the relative strength of coherency over a wider range of parameters than brief-presentation 2AFC methods, and exposed an oblique plaid effect in the entire range tested. There was no interaction between the effect of the global direction of motion and the effect of gratings' orientations. Thus, the oblique plaid effect is due to anisotropies inherent to motion mechanisms, not a bi-product of orientation anisotropies. The strong effect of a plaid's global direction on its tendency to cohere imposes new and important constraints on models of motion integration and transparency. Models that rely solely on relative differences in directions and/or orientations in the stimulus cannot predict our results. Instead, models should take into account anisotropies in the neuronal populations that represent the coherent percept (integrated motion) and those that represent the transparent percept (segmented motion). Furthermore, the oblique plaid effect could be used to test whether neuronal populations supposed to be involved in plaid perception display tuning biases in favor of cardinal directions.     

Percept-choice sequences driven by interrupted ambiguous stimuli: a low-level neural model

Existing neural explanations of spontaneous percept switching under steady viewing of an ambiguous stimulus do not fit the fact that stimulus interruptions cause the same percept to reappear across many ON/OFF cycles. We present a simple neural model that explains the observed behavior and predicts several more complicated percept sequences, without invoking any "high-level" decision making or memory. Percept choice at stimulus onset, which differs fundamentally from standard percept switching, depends crucially on a hitherto neglected interaction between local "shunting" adaptation and a near-threshold neural baseline. Stimulus ON/OFF timing then controls the generation of repeating, alternating, or more complex choice sequences. Our model also explains "priming" versus "habituation" effects on percept choice, reinterprets recent neurophysiological data, and predicts the emergence of hysteresis at the level of percept sequences, with occasional noise-induced sequence "hopping."     

Priming of pop-out on multiple time scales during visual search

When target-color repeats in pop-out visual search performance is faster than otherwise. While various characteristics of such priming of pop-out (PoP) are well known, relatively little is known about the temporal character of the memory traces underlying the effect. Recent findings on the perception of ambiguous stimuli show that the percept at any given moment is affected by perception over a long period, as well as by immediately preceding percepts. Intrigued by the existence of various parallels between this perceptual priming phenomenon and PoP, we here investigate whether similar multiplicity in timescales is seen for PoP. We contrasted long-term PoP build-up of a particular target color against shorter-term build-up for a different color. The priming effects from the two colors indeed reflect memory traces at different timescales: long-term priming build-up results in a more gradual decay than brief buildup, which is followed by faster decay. This is clearly demonstrated in Experiment 2 where sustained repetition of one target color is followed by a few repetitions of a second color. Following such a sequence, priming is initially stronger for the second target color, which was primed most recently; however, as more time passes longer-term priming starts to dominate, resulting in better search performance for the first color later on. Our results suggest that priming effects in visual search contain both transient and more sustained components. Similarities between the time courses of attentional priming and perception of ambiguous stimuli are striking and suggest compelling avenues of further research into the relation between the two effects.     

Extrinsic factors in the perception of bistable motion stimuli

When viewing a drifting plaid stimulus, perceived motion alternates over time between coherent pattern motion and a transparent impression of the two component gratings. It is known that changing the intrinsic attributes of such patterns (e.g. speed, orientation and spatial frequency of components) can influence percept predominance. Here, we investigate the contribution of extrinsic factors to perception; specifically contextual motion and eye movements. In the first experiment, the percept most similar to the speed and direction of surround motion increased in dominance, implying a tuned integration process. This shift primarily involved an increase in dominance durations of the consistent percept. The second experiment measured eye movements under similar conditions. Saccades were not associated with perceptual transitions, though blink rate increased around the time of a switch. This indicates that saccades do not cause switches, yet saccades in a congruent direction might help to prolong a percept because (i) more saccades were directionally congruent with the currently reported percept than expected by chance, and (ii) when observers were asked to make deliberate eye movements along one motion axis, this increased percept reports in that direction. Overall, we find evidence that perception of bistable motion can be modulated by information from spatially adjacent regions, and changes to the retinal image caused by blinks and saccades.     

Disambiguation of Necker cube rotation by monocular and binocular depth cues: relative effectiveness for establishing long-term bias

The apparent direction of rotation of perceptually bistable wire-frame (Necker) cubes can be conditioned to depend on retinal location by interleaving their presentation with cubes that are disambiguated by depth cues ( [Haijiang et al., 2006] and [Harrison and Backus, 2010a]). The long-term nature of the learned bias is demonstrated by resistance to counter-conditioning on a consecutive day. In previous work, either binocular disparity and occlusion, or a combination of monocular depth cues that included occlusion, internal occlusion, haze, and depth-from-shading, were used to control the rotation direction of disambiguated cubes. Here, we test the relative effectiveness of these two sets of depth cues in establishing the retinal location bias. Both cue sets were highly effective in establishing a perceptual bias on Day 1 as measured by the perceived rotation direction of ambiguous cubes. The effect of counter-conditioning on Day 2, on perceptual outcome for ambiguous cubes, was independent of whether the cue set was the same or different as Day 1. This invariance suggests that a common neural population instantiates the bias for rotation direction, regardless of the cue set used. However, in a further experiment where only disambiguated cubes were presented on Day 1, perceptual outcome of ambiguous cubes during Day 2 counter-conditioning showed that the monocular-only cue set was in fact more effective than disparity-plus-occlusion for causing long-term learning of the bias. These results can be reconciled if the conditioning effect of Day 1 ambiguous trials in the first experiment is taken into account (Harrison & Backus, 2010b). We suggest that monocular disambiguation leads to stronger bias either because it more strongly activates a single neural population that is necessary for perceiving rotation, or because ambiguous stimuli engage cortical areas that are also engaged by monocularly disambiguated stimuli but not by disparity-disambiguated stimuli.     

Voluntary control and the dynamics of perceptual bi-stability

Voluntary control and conscious perception seem to be related: when we are confronted with ambiguous images we are in some cases and to some extent able to voluntarily select a percept. However, to date voluntary control has not been used in neurophysiological studies on the correlates of conscious perception, presumably because the dynamic of perceptual reversals was not suitable. We exposed the visual system to four ambiguous stimuli that instigate bi-stable perception: slant rivalry, orthogonal grating rivalry, house-face rivalry, and Necker cube rivalry. In the preceding companion paper [van Ee, R. (2005). Dynamics of perceptual bi-stability for stereoscopic slant rivalry and a comparison with grating, house-face, and Necker cube rivalry. Vision Research] we focussed on the temporal dynamics of the perceptual reversals. Here we examined the role of voluntary control in the dynamics of perceptual reversals. We asked subjects to attempt to hold percepts and to speed-up the perceptual reversals. The investigations across the four stimuli revealed qualitative similarities concerning the influence of voluntary control on the temporal dynamics of perceptual reversals. We also found differences. In comparison to the other rivalry stimuli, slant rivalry exhibits: (1) relatively long percept durations; (2) a relatively clear role of voluntary control in modifying the percept durations. We advocate that these aspects, alongside with its metrical (quantitative) aspects, potentially make slant rivalry an interesting tool in studying the neural underpinnings of visual awareness.     

Online action-to-perception transfer: only percept-dependent action affects perception

Perception self-evidently affects action, but under which conditions does action in turn influence perception? To answer this question we ask observers to view an ambiguous stimulus that is alternatingly perceived as rotating clockwise or counterclockwise. When observers report the perceived direction by rotating a manipulandum, opposing directions between report and percept (‘incongruent’) destabilize the percept, whereas equal directions (‘congruent’) stabilize it. In contrast, when observers report their percept by key presses while performing a predefined movement, we find no effect of congruency. Consequently, our findings suggest that only percept-dependent action directly influences perceptual experience.     

First- and second-order processing in transient stereopsis

Large-field stimuli were used to investigate the interaction of first- and second-order pathways in transient-stereo processing. Stimuli consisted of sinewave modulations in either the mean luminance (first-order stimulus) or the contrast (second-order stimulus) of a dynamic-random-dot field. The main results of the present study are that: (1) Depth could be extracted with both the first-order and second-order stimuli; (2) Depth could be extracted from dichoptically mixed first- and second-order stimuli, however, the same stimuli, when presented as a motion sequence, did not result in a motion percept. Based upon these findings we conclude that the transient-stereo system processes both first- and second-order signals, and that these two signals are pooled prior to the extraction of transient depth. This finding of interaction between first- and second-order stereoscopic processing is different from the independence that has been found with the motion system.