Human parietal cortex structure predicts individual differences in perceptual rivalry.
ABSTRACT: When visual input has conflicting interpretations, conscious perception can alternate spontaneously between competing interpretations . There is a large amount of unexplained variability between individuals in the rate of such spontaneous alternations in perception [2-5]. We hypothesized that variability in perceptual rivalry might be reflected in individual differences in brain structure, because brain structure can exhibit systematic relationships with an individual's cognitive experiences and skills [6-9]. To test this notion, we examined in a large group of individuals how cortical thickness, local gray-matter density, and local white-matter integrity correlate with individuals' alternation rate for a bistable, rotating structure-from-motion stimulus . All of these macroscopic measures of brain structure consistently revealed that the structure of bilateral superior parietal lobes (SPL) could account for interindividual variability in perceptual alternation rate. Furthermore, we examined whether the bilateral SPL regions play a causal role in the rate of perceptual alternations by using transcranial magnetic stimulation (TMS) and found that transient disruption of these areas indeed decreases the rate of perceptual alternations. These findings demonstrate a direct relationship between structure of SPL and individuals' perceptual switch rate.
Project description:The posterior parietal cortex (PPC) is understood to be active when observers perceive three-dimensional (3D) structure. However, it is not clear how central this activity is in the construction of 3D spatial representations. Here, we examine whether PPC is essential for two aspects of visual depth perception by testing patients with lesions affecting this region. First, we measured subjects' ability to discriminate depth structure in various 3D surfaces and objects using binocular disparity. Patients with lesions to right PPC (N = 3) exhibited marked perceptual deficits on these tasks, whereas those with left hemisphere lesions (N = 2) were able to reliably discriminate depth as accurately as control subjects. Second, we presented an ambiguous 3D stimulus defined by structure from motion to determine whether PPC lesions influence the rate of bistable perceptual alternations. Patients' percept durations for the 3D stimulus were generally within a normal range, although the two patients with bilateral PPC lesions showed the fastest perceptual alternation rates in our sample. Intermittent stimulus presentation reduced the reversal rate similarly across subjects. Together, the results suggest that PPC plays a causal role in both inferring and maintaining the perception of 3D structure with stereopsis supported primarily by the right hemisphere, but do not lend support to the view that PPC is a critical contributor to bistable perceptual alternations.This article is part of the themed issue 'Vision in our three-dimensional world'.
Project description:When an ambiguous stimulus is viewed for a prolonged time, perception alternates between the different possible interpretations of the stimulus. The alternations seem haphazard, but closer inspection of their dynamics reveals systematic properties in many bistable phenomena. Parametric manipulations result in gradual changes in the fraction of time a given interpretation dominates perception, often over the entire possible range of zero to one. The mean dominance durations of the competing interpretations can also vary over wide ranges (from less than a second to dozens of seconds or more), but finding systematic relations in how they vary has proven difficult. Following the pioneering work of W. J. M. Levelt (1968) in binocular rivalry, previous studies have sought to formulate a relation in terms of the effect of physical parameters of the stimulus, such as image contrast in binocular rivalry. However, the link between external parameters and "stimulus strength" is not as obvious for other bistable phenomena. Here we show that systematic relations readily emerge when the mean dominance durations are examined instead as a function of "percept strength," as measured by the fraction of dominance time, and provide theoretical rationale for this observation. For three different bistable phenomena, plotting the mean dominance durations of the two percepts against the fraction of dominance time resulted in complementary curves with near-perfect symmetry around equi-dominance (the point where each percept dominates half the time). As a consequence, the alternation rate reaches a maximum at equi-dominance. We next show that the observed behavior arises naturally in simple double-well energy models and in neural competition models with cross-inhibition and input normalization. Finally, we discuss the possibility that bistable perceptual switches reflect a perceptual "exploratory" strategy, akin to foraging behavior, which leads naturally to maximal alternation rate at equi-dominance if perceptual switches come with a cost.
Project description:Bistable stimuli can give rise to two different interpretations between which our perception will alternate. Recent results showed a strong coupling between eye movements and reports of perceptual alternations with motion stimuli, which provides useful tools to objectively assess perceptual alternations. However, motion might entrain eye movements, and here we check with a static picture, the Necker cube, whether eye movements and perceptual reports (manual responses) reveal similar or different alternation rates, and similar or different sensitivity to attention manipulations. Using a cluster analysis, ocular temporal windows were defined based on the dynamics of ocular fixations during viewing of the Necker cube and compared to temporal windows extracted from manual responses. Ocular temporal windows were measured also with a control condition, where the physical stimulus presented to viewers alternated between two non-ambiguous versions of the Necker cube. Attention was manipulated by asking subjects to either report spontaneous alternations, focus on one percept, or switch as fast as possible between percepts. The validity of the ocular temporal windows was confirmed by the correspondence between ocular fixations when the physical stimulus changed and when the bistable Necker cube was presented. Ocular movements defined smaller time windows than time windows extracted from manual responses. The number of manual and ocular windows both increased between the spontaneous condition and the switch condition. However, only manual, and not ocular windows, increased in duration in the focus condition. Manual responses involve decisional mechanisms, and they may be decoupled from automatic oscillations between the two percepts, as suggested by the fact that both the number and duration of ocular windows remained stable between the spontaneous and focus conditions. In all, the recording of eye movements provides an objective measure of time windows, and reveals faster perceptual alternations with the Necker cube and less sensitivity to attention manipulations than manual responses.
Project description:During binocular rivalry, conflicting images presented to the two eyes compete for perceptual dominance, but the neural basis of this competition is disputed. In interocular switch rivalry, rival images periodically exchanged between the two eyes generate one of two types of perceptual alternation: (1) a fast, regular alternation between the images that is time-locked to the stimulus switches and has been proposed to arise from competition at lower levels of the visual processing hierarchy or (2) a slow, irregular alternation spanning multiple stimulus switches that has been associated with higher levels of the visual system. The existence of these two types of perceptual alternation has been influential in establishing the view that rivalry may be resolved at multiple hierarchical levels of the visual system. We varied the spatial, temporal, and luminance properties of interocular switch rivalry gratings and found, instead, an association between fast, regular perceptual alternations and processing by the magnocellular stream and between slow, irregular alternations and processing by the parvocellular stream. The magnocellular and parvocellular streams are two early visual pathways that are specialized for the processing of motion and form, respectively. These results provide a new framework for understanding the neural substrates of binocular rivalry that emphasizes the importance of parallel visual processing streams, and not only hierarchical organization, in the perceptual resolution of ambiguities in the visual environment.
Project description:When ambiguous visual stimuli have multiple interpretations, human perception can alternate between them, producing perceptual multistability. There is a large variation between individuals in how long stable percepts endure, on average, between switches, but the underlying neural basis of this individual difference in perceptual dynamics remains obscure. Here, we show that in one widely studied multistable paradigm-binocular rivalry-perceptual stability in individuals is predicted by the frequency of their neural oscillations within the alpha range (7-13?Hz). Our results suggest revising models of rivalry to incorporate effects of neural oscillations on perceptual alternations, and raise the possibility that a common factor may influence dynamics in many neural processes.
Project description:Binocular rivalry occurs when markedly different inputs to the two eyes initiate alternations in perceptual dominance between the two eyes' views. A link between individual differences in perceptual dynamics of rivalry and concentrations of GABA, a prominent inhibitory neurotransmitter in the brain, has highlighted binocular rivalry as a potential tool to investigate inhibitory processes in the brain. The present experiment investigated whether previously reported fluctuations of GABA concentrations in a healthy menstrual cycle (Epperson et al., 2002) also are associated with measurable changes in rivalry dynamics within individuals. We obtained longitudinal measures of alternation rate, dominance, and mixture durations in 300 rivalry tracking blocks measured over 5 weeks from healthy female participants who monitored the start of the follicular and luteal phases of their cycle. Although we demonstrate robust and stable individual differences in rivalry dynamics, across analytic approaches and dependent measures, we found no significant change or even trends across menstrual phases in the temporal dynamics of dominance percepts. We found only sparse between-phase differences in skew and kurtosis on mixture percepts when data were pooled across sessions and blocks. These results suggest a complex dynamic between hormonal steroids, binocular rivalry, and GABAeric signaling in the brain and thus implicate the need to consider a systemic perspective when linking GABA with perceptual alternations in binocular rivalry.
Project description:Visual cognition in humans has traditionally been studied with cognitive behavioral methods and brain imaging, but much less with genetic methods. Perceptual rivalry, an important phenomenon in visual cognition, is the spontaneous perceptual alternation that occurs between two distinct interpretations of a physically constant visual stimulus (e.g., binocular rivalry stimuli) or a perceptually ambiguous stimulus (e.g., the Necker cube). The switching rate varies dramatically across individuals and can be voluntarily modulated by observers. Here, we adopted a genomic approach to systematically investigate the genetics underlying binocular rivalry, Necker cube rivalry and voluntary modulation of Necker cube rivalry in young Chinese adults (Homo sapiens, 81% female, 20 ± 1 years old) at multiple levels, including common single nucleotide polymorphism (SNP)-based heritability estimation, SNP-based genome-wide association study (GWAS), gene-based analysis, and pathway analysis. We performed a pilot GWAS in 2441 individuals and replicated it in an independent cohort of 943 individuals. Common SNP-based heritability was estimated to be 25% for spontaneous perceptual rivalry. SNPs rs184765639 and rs75595941 were associated with voluntary modulation, and imaging data suggested genotypic difference of rs184765639 in the surface area of the left caudal-middle frontal cortex. Additionally, converging evidence from multilevel analyses associated genes such as PRMT1 with perceptual switching rate, and MIR1178 with voluntary modulation strength. In summary, this study discovered specific genetic contributions to perceptual rivalry and its voluntary modulation in human beings. These findings may promote our understanding of psychiatric disorders, as perceptual rivalry is a potential psychiatric biomarker.SIGNIFICANCE STATEMENT Perceptual rivalry is an important visual phenomenon in which our perception of a physically constant visual input spontaneously switches between two different states. There are individual variations in perceptual switching rate and voluntary modulation strength. Our genomic analyses reveal several loci associated with these two kinds of variation. Because perceptual rivalry is thought to be relevant to and potentially an endophenotype for psychiatric disorders, these results may help understand not only visual cognition, but also psychiatric disorders.
Project description:Slowing of the rate at which a rivalrous percept switches from one configuration to another has been suggested as a potential trait marker for bipolar disorder. We measured perceptual alternations for a bistable, rotating, structure-from-motion cylinder in bipolar and control participants. In a control task, binocular depth rendered the direction of cylinder rotation unambiguous to monitor participants' performance and attention during the experimental task. A particular direction of rotation was perceptually stable, on average, for 33.5s in participants without psychiatric diagnosis. Euthymic, bipolar participants showed a slightly slower rate of switching between the two percepts (percept duration 42.3s). Under a parametric analysis of the best-fitting model for individual participants, this difference was statistically significant. However, the variability within groups was high, so this difference in average switch rates was not big enough to serve as a trait marker for bipolar disorder. We also found that low-level visual capacities, such as stereo threshold, influence perceptual switch rates. We suggest that there is no single brain location responsible for perceptual switching in all different ambiguous figures and that perceptual switching is generated by the actions of local cortical circuitry.
Project description:BACKGROUND:During observation of the Necker cube perception becomes unstable and alternates repeatedly between a from-above-perspective ("fap") and a from-below-perspective ("fbp") interpretation. Both interpretations are physically equally plausible, however, observers usually show an a priori top-down bias in favor of the fap interpretation. Patients with Autism spectrum disorder are known to show an altered pattern of perception with a focus on sensory details. In the present study we tested whether this altered perceptual processing affects their reversal dynamics and reduces the perceptual bias during Necker cube observation. METHODS:19 participants with Asperger syndrome and 16 healthy controls observed a Necker cube stimulus continuously for 5 minutes and indicated perceptual reversals by key press. We compared reversal rates (number of reversals per minute) and the distributions of dwell times for the two interpretations between observer groups. RESULTS:Asperger participants showed less perceptual reversal than controls. Six Asperger participants did not perceive any reversal at all, whereas all observers from the control group perceived at least five reversals within the five minutes observation time. Further, control participants showed the typical perceptual bias with significant longer median dwell times for the fap compared to the fbp interpretation. No such perceptual bias was found in the Asperger group. DISCUSSION:The perceptual system weights the incomplete and ambiguous sensory input with memorized concepts in order to construct stable and reliable percepts. In the case of the Necker cube stimulus, two perceptual interpretations are equally compatible with the sensory information and internal fluctuations may cause perceptual alternations between them-with a slightly larger probability value for the fap interpretation (perceptual bias). Smaller reversal rates in Asperger observers may result from the dominance of bottom-up sensory input over endogenous top-down factors. The latter may also explain the absence of a fap bias.
Project description:During perceptual rivalry, an observer's perceptual experience alternates over time despite constant sensory stimulation. Perceptual alternations are thought to be driven by conflicting or ambiguous retinal image features at a particular spatial location and modulated by global context from surrounding locations. However, rivalry can also occur between two illusory stimuli-such as two filled-in stimuli within the retinal blind spot. In this "filling-in rivalry," what observers perceive in the blind spot changes in the absence of local stimulation. It remains unclear if filling-in rivalry shares common mechanisms with other types of rivalry. We measured the dynamics of rivalry between filled-in percepts in the blind spot, finding a high degree of exclusivity (perceptual dominance of one filled-in percept, rather than a perception of transparency), alternation rates that were highly consistent for individual observers, and dynamics that closely resembled other forms of perceptual rivalry. The results suggest that mechanisms common to a wide range of rivalry situations need not rely on conflicting retinal image signals.