When two dissimilar stimuli are presented to the eyes, perception alternates between multiple interpretations, a phenomenon dubbed binocular rivalry. Numerous recent imaging studies have attempted to unveil neural substrates underlying multistable perception. However, these studies had a conceptual constraint: access to observers' perceptual state relied on their introspection and active report. Here, we investigated to what extent neural correlates of binocular rivalry in healthy humans are confounded by this subjective measure and by action. We used the optokinetic nystagmus and pupil size to objectively and continuously map perceptual alternations for binocular-rivalry stimuli. Combining these two measures with fMRI allowed us to assess the neural correlates of binocular rivalry time locked to the perceptual alternations in the absence of active report. When observers were asked to actively report their percept, our objective measures matched the report. In this active condition, objective measures and subjective reporting revealed that occipital, parietal, and frontal areas underlie the processing of binocular rivalry, replicating earlier findings. Furthermore, objective measures provided additional statistical power due to their continuous nature. Importantly, when observers passively experienced rivalry without reporting perceptual alternations, a different picture emerged: differential neural activity in frontal areas was absent, whereas activation in occipital and parietal regions persisted. Our results question the popular view of a driving role of frontal areas in the initiation of perceptual alternations during binocular rivalry. Instead, we conclude that frontal areas are associated with active report and introspection rather than with rivalry per se.
Imitation typically occurs in social contexts where people interact and have common goals. Here, we show that people are also highly susceptible to imitate each other in a competitive context. Pairs of players performed a competitive and fast-reaching task (a variant of the arcade whac-a-mole game) in which money could be earned if players hit brief-appearing visual targets on a large touchscreen before their opponents. In three separate experiments, we demonstrate that reaction times and movements were highly correlated within pairs of players. Players affected their success by imitating each other, and imitation depended on the visibility of the opponents behavior. Imitation persisted, despite the competitive and demanding nature of the game, even if this resulted in lower scores and payoffs and even when there was no need to counteract the opponents actions.
The link between arousal and pupil dilation is well studied, but it is less known that other cognitive processes can trigger pupil responses. Here we present evidence that pupil responses can be induced by high-level scene processing, independent of changes in low-level features or arousal. In Experiment 1, we recorded changes in pupil diameter of observers while they viewed a variety of natural scenes with or without a sun that were presented either upright or inverted. Image inversion had the strongest effect on the pupil responses. The pupil constricted more to the onset of upright images as compared to inverted images. Furthermore, the amplitudes of pupil constrictions to viewing images containing a sun were larger relative to control images. In Experiment 2, we presented cartoon versions of upright and inverted pictures that included either a sun or a moon. The image backgrounds were kept identical across conditions. Similar to Experiment 1, upright images triggered pupil constrictions with larger amplitudes than inverted images and images of the sun evoked greater pupil contraction than images of the moon. We suggest that the modulations of pupil responses were due to higher-level interpretations of image content.
Declarative memories of personal experiences are a key factor in defining oneself as an individual, which becomes particularly evident when this capability is impaired. Assessing the physiological mechanisms of human declarative memory is typically restricted to patients with specific lesions and requires invasive brain access or functional imaging. We investigated whether the pupil, an accessible physiological measure, can be utilized to probe memories for complex natural visual scenes. During memory encoding, scenes that were later remembered elicited a stronger pupil constriction compared to scenes that were later forgotten. Thus, pupil size predicts success or failure of memory formation. In contrast, novel scenes elicited stronger pupil constriction than familiar scenes during retrieval. When viewing previously memorized scenes, those that were forgotten (misjudged as novel) still elicited stronger pupil constrictions than those correctly judged as familiar. Furthermore, pupil constriction was influenced more strongly if images were judged with high confidence. Thus, we propose that pupil constriction can serve as a marker of novelty. Since stimulus novelty modulates the efficacy of memory formation, our pupil measurements during learning indicate that the later forgotten images were perceived as less novel than the later remembered pictures. Taken together, our data provide evidence that pupil constriction is a physiological correlate of a neural novelty signal during formation and retrieval of declarative memories for complex, natural scenes.
The muscles that control the pupil are richly innervated by the autonomic nervous system. While there are central pathways that drive pupil dilations in relation to arousal, there is no anatomical evidence that cortical centers involved with visual selective attention innervate the pupil. In this study, we show that such connections must exist. Specifically, we demonstrate a novel Pupil Frequency Tagging (PFT) method, where oscillatory changes in stimulus brightness over time are mirrored by pupil constrictions and dilations. We find that the luminance-induced pupil oscillations are enhanced when covert attention is directed to the flicker stimulus and when targets are correctly detected in an attentional tracking task. These results suggest that the amplitudes of pupil responses closely follow the allocation of focal visual attention and the encoding of stimuli. PFT provides a new opportunity to study top-down visual attention itself as well as identifying the pathways and mechanisms that support this unexpected phenomenon.
Pupil dilation is implicated as a marker of decision-making as well as of cognitive and emotional processes. Here we tested whether individuals can exploit anothers pupil to their advantage. We first recorded the eyes of 3 "opponents", while they were playing a modified version of the "rock-paper-scissors" childhood game. The recorded videos served as stimuli to a second set of participants. These "players" played rock-paper-scissors against the pre-recorded opponents in a variety of conditions. When players just observed the opponents eyes without specific instruction their probability of winning was at chance. When informed that the time of maximum pupil dilation was indicative of the opponents choice, however, players raised their winning probability significantly above chance. When just watching the reconstructed area of the pupil against a gray background, players achieved similar performance, showing that players indeed exploited the pupil, rather than other facial cues. Since maximum pupil dilation was correct about the opponents decision only in 60% of trials (chance 33%), we finally tested whether increasing this validity to 100% would allow spontaneous learning. Indeed, when players were given no information, but the pupil was informative about the opponents response in all trials, players performed significantly above chance on average and half (5/10) reached significance at an individual level. Together these results suggest that people can in principle use the pupil to detect cognitive decisions in another individual, but that most people have neither explicit knowledge of the pupils utility nor have they learnt to use it despite a lifetime of exposure.
Rivalry is a common tool to probe visual awareness: a constant physical stimulus evokes multiple, distinct perceptual interpretations ("percepts") that alternate over time. Percepts are typically described as mutually exclusive, suggesting that a discrete (all-or-none) process underlies changes in visual awareness. Here we follow two strategies to address whether rivalry is an all-or-none process: first, we introduce two reflexes as objective measures of rivalry, pupil dilation and optokinetic nystagmus (OKN); second, we use a continuous input device (analog joystick) to allow observers a gradual subjective report. We find that the "reflexes" reflect the percept rather than the physical stimulus. Both reflexes show a gradual dependence on the time relative to perceptual transitions. Similarly, observers joystick deflections, which are highly correlated with the reflex measures, indicate gradual transitions. Physically simulating wave-like transitions between percepts suggest piece-meal rivalry (i.e., different regions of space belonging to distinct percepts) as one possible explanation for the gradual transitions. Furthermore, the reflexes show that dominance durations depend on whether or not the percept is actively reported. In addition, reflexes respond to transitions with shorter latencies than the subjective report and show an abundance of short dominance durations. This failure to report fast changes in dominance may result from limited access of introspection to rivalry dynamics. In sum, reflexes reveal that rivalry is a gradual process, rivalrys dynamics is modulated by the required action (response mode), and that rapid transitions in perceptual dominance can slip away from awareness.
Object-based attention facilitates the processing of features that form the object. Two hypotheses are conceivable for how object-based attention is deployed to an objects features: first, the object is attended by selecting its features; alternatively, a configuration of features as such is attended by selecting the object representation they form. Only for the latter alternative, the perception of a feature configuration as entity ("objecthood") is a necessary condition for object-based attention. Disentangling the two alternatives requires the comparison of identical feature configurations that induce the perception of an object in one condition ("bound") and do not do so in another condition ("unbound"). We used an ambiguous stimulus, whose percept spontaneously switches between bound and unbound, while the stimulus itself remains unchanged. We tested discrimination on the boundary of the diamond as well as detection of probes inside and outside the diamond. We found discrimination performance to be increased if features were perceptually bound into an object. Furthermore, detection performance was higher within and lower outside the bound object as compared to the unbound configuration. Consequently, the facilitation of processing by object-based attention requires objecthood, that is, a unified internal representation of an "object"-not a mere collection of features.
In rivalry, constant stimuli allow several interpretations ("percepts"). Percepts are characterized by their probability to occur and by the duration of their dominance. During continuous presentation of bi-stable stimuli, both percept probabilities are trivially 50%. To disentangle the processes triggering a percept from those stabilizing it, we introduce tri-stable stimuli having three percepts. We find the probability and dominance duration of a percept independently adjustable. Percept probabilities and dominance durations show mutual dependencies across several perceptual switches. Consequently, the current perceptual experience depends on perceptual history; therefore, rivalry--even for continuous presentation--is not a memory-less process.
We used binocular rivalry and generalized flash suppression to identify several new shared properties of traveling suppression waves. A strong relationship was found between suppression wave speed and induction pulse strength: increasing the contrast or dot density of the induction pulse led to an increase in wave speed. Evidence of visual field anisotropies in wave propagation speeds were also seen, with suppression waves decelerating as they travel towards the fovea. This deceleration could not be accounted for by cortical magnification in lower level brain areas, suggesting an important role for other, yet to be identified, factors.
Humans process natural scenes rapidly and accurately. Low-level image features and emotional valence affect such processing but have mostly been studied in isolation. At which processing stage these factors operate and how they interact has remained largely unaddressed. Here, we briefly presented natural images and asked observers to report the presence or absence of an animal (detection), species of the detected animal (identification), and their confidence. In a second experiment, the same observers rated images with respect to their emotional affect and estimated their anxiety when imagining a real-life encounter with the depicted animal. We found that detection and identification improved with increasing image luminance, background contrast, animal saturation, and luminance plus color contrast between target and background. Surprisingly, animals associated with lower anxiety were detected faster and identified with higher confidence, and emotional affect was a better predictor of performance than anxiety. Pupil size correlated with detection, identification, and emotional valence judgments at different time points after image presentation. Remarkably, images of threatening animals induced smaller pupil sizes, and observers with higher mean anxiety ratings had smaller pupils on average. In sum, rapid visual processing depends on contrasts between target and background features rather than overall visual context, is negatively affected by anxiety, and finds its processing stages differentially reflected in the pupillary response.
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