FMRI-based decoding of reward effects in binocular rivalry.
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ABSTRACT:
SUBMITTER: Wilbertz G
PROVIDER: S-EPMC6007140 | biostudies-literature | 2017
REPOSITORIES: biostudies-literature
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Project description:Perception is an inferential process, which becomes immediately evident when sensory information is conflicting or ambiguous and thus allows for more than one perceptual interpretation. Thinking the idea of perception as inference through to the end results in a blurring of boundaries between perception and action selection, as perceptual inference implies the construction of a percept as an active process. Here we therefore wondered whether perception shares a key characteristic of action selection, namely that it is shaped by reinforcement learning. In two behavioral experiments, we used binocular rivalry to examine whether perceptual inference can be influenced by the association of perceptual outcomes with reward or punishment, respectively, in analogy to instrumental conditioning. Binocular rivalry was evoked by two orthogonal grating stimuli presented to the two eyes, resulting in perceptual alternations between the two gratings. Perception was tracked indirectly and objectively through a target detection task, which allowed us to preclude potential reporting biases. Monetary reward or punishments were given repeatedly during perception of only one of the two rivaling stimuli. We found an increase in dominance durations for the percept associated with reward, relative to the non-rewarded percept. In contrast, punishment led to an increase of the non-punished compared to a relative decrease of the punished percept. Our results show that perception shares key characteristics with action selection, in that it is influenced by reward and punishment in opposite directions, thus narrowing the gap between the conceptually separated domains of perception and action selection. We conclude that perceptual inference is an adaptive process that is shaped by its consequences.
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Project description:An interocular conflict arises when different images are presented to each eye at the same spatial location. The visual system resolves this conflict through binocular rivalry: observers consciously perceive spontaneous alternations between the two images. Visual attention is generally important for resolving competition between neural representations. However, given the seemingly spontaneous and automatic nature of binocular rivalry, the role of attention in resolving interocular competition remains unclear. Here we test whether visual attention is necessary to produce rivalry. Using an EEG frequency-tagging method to track cortical representations of the conflicting images, we show that when attention was diverted away, rivalry stopped. The EEG data further suggested that the neural representations of the dichoptic images combined without attention. Thus, attention is necessary for dichoptic images to be engaged in sustained rivalry and may be generally required for resolving conflicting, potentially ambiguous input and giving a single interpretation access to consciousness.
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Project description:When two incompatible images are shown separately to each eye, a perceptual process known as binocular rivalry occurs by which the two images compete for awareness. The site of competition for binocular rivalry has been a topic of debate, and recent theories are that it may occur either at low levels of the visual system where the inputs from the two eyes are combined or at high levels of the visual system where the two images are processed. One of the major pieces of evidence for a high-level image account of rivalry is a phenomenon known as stimulus rivalry, in which two competing stimuli are swapped between the eyes at 3 Hz. However, there is little available neurophysiological evidence for a neural substrate for this high-level competition. Here, we used frequency tagging of two competing stimuli in binocular rivalry and stimulus rivalry in humans to evaluate whether the steady-state visually evoked potentials (SSVEPs) show similar signatures of neural competition for both conditions. We found that flickering the stimuli generates spectral power at the tagged frequencies in both types of rivalry in the early visual cortex. We then quantified dynamic signatures of competition by tracking amplitude changes in the frequency tags, which showed that both types of rivalry colocalized in occipital regions of the cortex. Thus, contrary to our hypothesis that stimulus rivalry was being mediated by high-level competition between the images, we find that neural competition measured by the SSVEP instead suggests that the sites of competition for stimulus rivalry and binocular rivalry may similarly include the occipital pole and middle temporal gyrus (hMT+/V5) of the visual system, consistent with a low-level, binocular interpretation.
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Project description:Vision is widely accepted as the dominant sense in larger primates including humans, whereas olfaction is often considered a vestigial sense yielding only obscure object representations [1]. It is well documented that vision drives olfactory perception [2, 3], but there has been little indication that olfaction could modulate visual perception. Here we introduce smells to a well-established visual phenomenon termed binocular rivalry, perceptual alternations that occur when distinctively different images are separately presented to the two eyes [4]. We show that an odorant congruent to one of the competing images prolongs the time that image is visible and shortens its suppression time in a manner that is automatic, essentially independent of cognitive control, and partly subconscious. Our findings provide the first direct evidence that an olfactory cue biases the dynamic process of binocular rivalry, thereby demonstrating olfactory modulation of visual perception-an effect that has been hitherto unsuspected.
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Project description:During binocular-rivalry suppression, an ordinarily visible stimulus is erased from awareness, but how is the sensory representation of that stimulus affected? Although it is established that rivalry suppression attenuates signal strength, the influence of suppression on signal fidelity remains unknown. Here, we show that noise plays a hitherto undiscovered role in the degradation of the percept under suppression. In Experiment 1, we measured psychometric functions for a stimulus presented under dominance and suppression, and found that the slope of these functions was shallower under suppression-a result suggesting that the signal representation was rendered noisier. Experiment 2 then revealed the source of this noise: An examination of the influence of suppression on the orientation bandwidth of noise masking showed that tuning bandwidth is significantly broadened under suppression. Thus, the discriminability of a suppressed stimulus is weakened not only by a general decrease in signal strength, but also by broader orientation tuning that introduces more noise in the neural representation of the suppressed stimulus.
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Project description:Binocular rivalry is a phenomenon in which perception spontaneously shifts between two different images that are dichoptically presented to the viewer. By elucidating the cortical networks responsible for these stochastic fluctuations in perception, we can potentially learn much about the neural correlates of visual awareness. We obtained concurrent EEG-fMRI data for a group of 20 healthy human subjects during the continuous presentation of dichoptic visual stimuli. The two eyes' images were tagged with different temporal frequencies so that eye specific steady-state visual evoked potential (SSVEP) signals could be extracted from the EEG data for direct comparison with changes in fMRI BOLD activity associated with binocular rivalry. We additionally included a smooth replay condition that emulated the perceptual transitions experienced during binocular rivalry as a control stimulus. We evaluated a novel SSVEP-informed fMRI analysis in this study in order to delineate the temporal dynamics of rivalry-related BOLD activity from both an electrophysiological and behavioral perspective. In this manner, we assessed BOLD activity during rivalry that was directly correlated with peaks and crosses of the two rivaling, frequency-tagged SSVEP signals, for comparison with BOLD activity associated with subject reported perceptual transitions. Our findings point to a critical role of a right lateralized fronto-parietal network in the processing of bistable stimuli, given that BOLD activity in the right superior/inferior parietal lobules was significantly elevated throughout binocular rivalry and in particular during perceptual transitions, compared with the replay condition. Based on the SSVEP-informed analysis, rivalry was further associated with significantly enhanced BOLD suppression in the posterior mid-cingulate cortex during perceptual transitions, compared with SSVEP crosses. Overall, this work points to a careful interplay between early visual areas, the right posterior parietal cortex and the mid-cingulate cortex in mediating the spontaneous perceptual changes associated with binocular rivalry and has significant implications for future multimodal imaging studies of perception and awareness.
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Project description:During binocular rivalry, physical stimulation is dissociated from conscious visual awareness. Human brain imaging reveals a tight linkage between the neural events in human primary visual cortex (V1) and the dynamics of perceptual waves during transitions in dominance during binocular rivalry. Here, we report results from experiments in which observers' attention was diverted from the rival stimuli, implying that: competition between two rival stimuli involves neural circuits in V1, and attention is crucial for the consequences of this neural competition to advance to higher visual areas and promote perceptual waves.
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Project description:Faces are important visual objects for humans and other social animals. A complex network of specialized brain areas is involved in the recognition and interpretation of faces. This network needs to strike a balance between being sensitive enough to distinguish between different faces with similar features, and being tolerant of low-level visual changes so that a given face is stably perceived as a particular individual. Such stability may require feedback from higher brain regions down to the level where details are represented. Here, we describe a phenomenon in which interocular competition between face features is stabilized and eliminated when observers attend high-level face characteristics. Two different face images presented to the individual eyes do not cause the perceptual fluctuations that are typically observed in binocular rivalry. Instead, they merge into a stable percept of an intermediate face that combines features from both eyes' images. The stability of the intermediate face percept depends on the observer attending holistic face properties such as identity or gender. It disappears when observers explicitly attend facial features, suggesting a crucial role of top-down stabilizing feedback from high-level areas that represent holistic faces back to lower processing levels where detailed face features compete for conscious representation.
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Project description:PurposeWe sought brain activity that predicts visual consciousness.MethodsWe used electroencephalography (EEG) to measure brain activity to a 1000-ms display of sine-wave gratings, oriented vertically in one eye and horizontally in the other. This display yields binocular rivalry: irregular alternations in visual consciousness between the images viewed by the eyes. We replaced both gratings with 200 ms of darkness, the gap, before showing a second display of the same rival gratings for another 1000 ms. We followed this by a 1000-ms mask then a 2000-ms inter-trial interval (ITI). Eleven participants pressed keys after the second display in numerous trials to say whether the orientation of the visible grating changed from before to after the gap or not. Each participant also responded to numerous non-rivalry trials in which the gratings had identical orientations for the two eyes and for which the orientation of both either changed physically after the gap or did not.ResultsWe found that greater activity from lateral occipital-parietal-temporal areas about 180 ms after initial onset of rival stimuli predicted a change in visual consciousness more than 1000 ms later, on re-presentation of the rival stimuli. We also found that less activity from parietal, central, and frontal electrodes about 400 ms after initial onset of rival stimuli predicted a change in visual consciousness about 800 ms later, on re-presentation of the rival stimuli. There was no such predictive activity when the change in visual consciousness occurred because the stimuli changed physically.ConclusionWe found early EEG activity that predicted later visual consciousness. Predictive activity 180 ms after onset of the first display may reflect adaption of the neurons mediating visual consciousness in our displays. Predictive activity 400 ms after onset of the first display may reflect a less-reliable brain state mediating visual consciousness.
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Project description:Visually identifying glossy surfaces can be crucial for survival (e.g. ice patches on a road), yet estimating gloss is computationally challenging for both human and machine vision. Here, we demonstrate that human gloss perception exploits some surprisingly simple binocular fusion signals, which are likely available early in the visual cortex. In particular, we show that the unusual disparity gradients and vertical offsets produced by reflections create distinctive 'proto-rivalrous' (barely fusible) image regions that are a critical indicator of gloss. We find that manipulating the gradients and vertical components of binocular disparities yields predictable changes in material appearance. Removing or occluding proto-rivalrous signals makes surfaces look matte, while artificially adding such signals to images makes them appear glossy. This suggests that the human visual system has internalized the idiosyncratic binocular fusion characteristics of glossy surfaces, providing a straightforward means of estimating surface attributes using low-level image signals.
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