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Helmholtz asked whether one could discriminate which eye is the origin of one's perception merely based on the retinal signals. Studies to date showed that participants' ability to tell the eye-of-origin most likely depends on contextual cues. Nevertheless, it has been shown that exogenous attention can enhance performance for monocularly presented stimuli. We questioned whether adults can be trained to discriminate the eye-of-origin of their perceptions and if this ability depends on the strength of the monocular channels. We used attentional feed-forward training to improve the subject's eye-of-origin discrimination performance with voluntary attention. During training, participants received a binocular cue to inform them of the eye-of-origin of an upcoming target. Using continuous flash suppression, we also measured the signal strength of the monocular targets to see any possible modulations related to the cues. We collected confidence ratings from the participants about their eye-of-origin judgements to study in further detail whether metacognition has access to this information. Our results show that, even though voluntary attention did not alter the strength of the monocular channels, eye-of-origin discrimination performance improved following the training. A similar pattern was observed for confidence. The results from the feedforward attentional training and the increase in subjective confidence point towards a high-level decisional mechanism being responsible for the eye-of-origin judgements. We propose that this high-level process is informed by subtle sensory cues such as the differences in luminance or contrast in the two monocular channels.
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Atenção , Percepção Visual , Humanos , Atenção/fisiologia , Adulto , Masculino , Feminino , Percepção Visual/fisiologia , Adulto Jovem , Sinais (Psicologia) , Estimulação Luminosa/métodos , Visão Monocular/fisiologia , Visão Binocular/fisiologia , Discriminação Psicológica/fisiologiaRESUMO
Binocular rivalry is a widely used tool in sensory and cognitive neuroscience to investigate different aspects of vision and cognition. The dynamics of binocular rivalry (e.g., duration of perceptual dominance phases and mixed percept proportions) differ across individuals; based on rivalry dynamics, it is also possible to calculate an index of ocular dominance (by comparing the perceptual dominance of the images in the two eyes). In this study, we investigated the reliability of binocular rivalry dynamics using different methods for dichoptic stimulation and different rivalry stimuli. For the three main indices we defined (ocular dominance, phase durations and mixed percept proportions), we found a high test-retest reliability across sessions. Moreover, the test-retest reliability of the ocular dominance index was predictable from its internal consistency, supporting its stability over time. Phase durations and mixed percept proportions, in contrast, had worse test-retest reliability than expected based on internal consistency, indicating that these parameters are susceptible to state-dependent changes. Our results support the use of the ocular dominance index and binocular rivalry in the measurement of sensory eye dominance and its plasticity, but advise caution when investigating the association between phase durations or mixed percepts and stable characteristics like psychological traits or disorders.
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Cognição , Dominância Ocular , Humanos , Reprodutibilidade dos Testes , OlhoRESUMO
Neuroplasticity is maximal during development and declines in adulthood, especially for sensory cortices. On the other hand, the motor and prefrontal cortices retain plasticity throughout the lifespan. This difference has led to a modular view of plasticity in which different brain regions have their own plasticity mechanisms that do not depend or translate on others. Recent evidence shows that visual and motor plasticity share common neural mechanisms (e.g., GABAergic inhibition), indicating a possible link between these different forms of plasticity, however, the interaction between visual and motor plasticity has never been tested directly. Here, we show that when visual and motor plasticity are elicited at the same time in adult humans, visual plasticity is impaired, while motor plasticity is spared. Moreover, simultaneous activation of working memory and visual plasticity also leads to impairment in visual plasticity. These unilateral interactions between visual, working memory, and motor plasticity demonstrate a clear link between these three forms of plasticity. We conclude that local neuroplasticity in separate systems might be regulated globally, to preserve overall homeostasis in the brain.
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Dominância Ocular , Privação Sensorial , Humanos , Adulto , Privação Sensorial/fisiologia , Inibição Psicológica , Encéfalo , Plasticidade Neuronal/fisiologia , Memória de Curto PrazoRESUMO
The ocular dominance shift observed after short-term monocular deprivation is a widely used measure of visual homeostatic plasticity in adult humans. Binocular rivalry and binocular combination techniques are used interchangeably to characterize homeostatic plasticity, sometimes leading to contradictory results. Here we directly compare the effect of short-term monocular deprivation on ocular dominance measured by either binocular rivalry or binocular combination and its dependence on the duration of deprivation (15 or 120 min) in the same group of participants. Our results show that both binocular rivalry and binocular combination provide reliable estimates of ocular dominance, which are strongly correlated across techniques both before and after deprivation. Moreover, while 15 min of monocular deprivation induce a larger shift of ocular dominance when measured using binocular combination compared to binocular rivalry, for both techniques, the shift in ocular dominance exhibits a strong dependence on the duration of monocular deprivation, with longer deprivation inducing a larger and longer-lasting shift in ocular dominance. Taken together, our results indicate that both binocular rivalry and binocular combination offer very consistent and reliable measurements of both ocular dominance and the effect short-term monocular deprivation.
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Dominância Ocular , Plasticidade Neuronal , Adulto , Humanos , Visão Binocular , Visão MonocularRESUMO
Monetary value enhances visual perception and attention and boosts activity in the primary visual cortex, however, it is still unclear whether monetary value can modulate the conscious access to rewarding stimuli. Here we investigate this issue by employing a breaking continuous flash suppression (b-CFS) paradigm. We measured suppression durations of sinusoidal gratings having orthogonal orientations under CFS in adult volunteers before and after a short session of Pavlovian associative learning in which each orientation was arbitrarily associated either with high or low monetary reward. We found that monetary value accelerated the access to visual awareness during CFS. Specifically, after the associative learning, suppression durations of the visual stimulus associated with high monetary value were shorter compared to the visual stimulus associated with low monetary value. Critically, the effect was replicated in a second experiment using a detection task for b-CFS that was orthogonal to the reward associative learning. These results indicate that monetary reward facilitates the access to awareness of visual stimuli associated with monetary value probably by boosting their representation at the early stages of visual processing in the brain.
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Conscientização , Adulto , Humanos , Aprendizagem , Atenção , Percepção Visual , Estimulação Luminosa/métodosRESUMO
Moderate physical activity can influence cognitive functions and visual cortical activity. However, little is known about the effects of exercise on fundamental perceptual domains, such as spatial and temporal representation. Here we tackled this issue by testing the impact of physical activity on a temporal estimation task in a group of adult volunteers in three different conditions: (1) in a resting condition (baseline), (2) during moderate physical activity (cycling in place - PA), and (3) approximately 15 to 20 min following the physical activity phase, in which participants were seated and returned to a regular heart rate (POST). We show that physical activity specifically impacts time perception, inducing a consistent overestimation for durations in the range of milliseconds. Notably, the effect persisted in the POST session, ruling out the main contribution of either heart rate or cycling rhythmicity. In a control experiment, we found that spatial perception (distance estimation) was unaffected by physical activity, ruling out a major contribution of arousal and fatigue to the observed temporal distortion. We speculate that physical exercise might alter temporal estimation either by up-regulating the dopaminergic system or modulating GABAergic inhibition.
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Sleep and plasticity are highly interrelated, as sleep slow oscillations and sleep spindles are associated with consolidation of Hebbian-based processes. However, in adult humans, visual cortical plasticity is mainly sustained by homeostatic mechanisms, for which the role of sleep is still largely unknown. Here, we demonstrate that non-REM sleep stabilizes homeostatic plasticity of ocular dominance induced in adult humans by short-term monocular deprivation: the counterintuitive and otherwise transient boost of the deprived eye was preserved at the morning awakening (>6 hr after deprivation). Subjects exhibiting a stronger boost of the deprived eye after sleep had increased sleep spindle density in frontopolar electrodes, suggesting the involvement of distributed processes. Crucially, the individual susceptibility to visual homeostatic plasticity soon after deprivation correlated with the changes in sleep slow oscillations and spindle power in occipital sites, consistent with a modulation in early occipital visual cortex.
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Dominância Ocular , Córtex Visual , Adulto , Eletroencefalografia , Humanos , Plasticidade Neuronal , SonoRESUMO
We used pupillometry to evaluate the effects of attention cueing on perceptual bi-stability, as reported by adult human observers. Perceptual alternations and pupil diameter were measured during two forms of rivalry, generated by presenting a white and a black disk to the two eyes (binocular rivalry) or splitting the disks between eyes (interocular grouping rivalry). In line with previous studies, we found that subtle pupil size modulations (about 0.05 mm) tracked alternations between exclusive dominance phases of the black or white disk. These pupil responses were larger for perceptually stronger stimuli: presented to the dominant eye or with physically higher luminance contrast. However, cueing of endogenous attention to one of the rivaling percepts did not affect pupil modulations during exclusive dominance phases. This was observed despite the reliable effects of endogenous attention on perceptual dominance, which shifted in favor of the cued percept by about 10%. The results were comparable for binocular and interocular grouping rivalry. Cueing only had a marginal modulatory effect on pupil size during mixed percepts in binocular rivalry. This may suggest that, rather than acting by modulating perceptual strength, endogenous attention primarily acts during periods of unresolved competition, which is compatible with attention being automatically directed to the rivaling stimuli during periods of exclusive dominance and thereby sustaining perceptual alternations.Significance StatementBinocular rivalry depends on attention. When it is diverted away from the stimuli, perceptual alternations slow down; when it is preferentially directed to one stimulus, perception lingers more on it, consistent with attention enhancing the effective strength of the rivaling stimuli. Here we introduce pupillometry as a means to indirectly track changes in effective stimulus strength. We find that pupil size accurately tracks perceived luminance during two forms of rivalry: binocular rivalry and interocular grouping rivalry. Both show robust effects of attention cueing on perceptual dominance, but pupil modulations during exclusive dominance are unaffected by cueing. This suggests that endogenous attention does not affect perceptual strength during exclusive dominance, though it might do so during transition phases.
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While there is evidence that the visual cortex retains a potential for plasticity in adulthood, less is known about the subcortical stages of visual processing. Here, we asked whether short-term ocular dominance plasticity affects the human visual thalamus. We addressed this question in normally sighted adult humans, using ultra-high field (7T) magnetic resonance imaging combined with the paradigm of short-term monocular deprivation. With this approach, we previously demonstrated transient shifts of perceptual eye dominance and ocular dominance in visual cortex (Binda et al., 2018). Here, we report evidence for short-term plasticity in the ventral division of the pulvinar (vPulv), where the deprived eye representation was enhanced over the nondeprived eye. This vPulv plasticity was similar as previously seen in visual cortex and it was correlated with the ocular dominance shift measured behaviorally. In contrast, there was no effect of monocular deprivation in two adjacent thalamic regions: dorsal pulvinar and Lateral Geniculate Nucleus. We conclude that the visual thalamus retains potential for short-term plasticity in adulthood; the plasticity effect differs across thalamic subregions, possibly reflecting differences in their corticofugal connectivity.
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Visão Monocular , Córtex Visual , Adulto , Dominância Ocular , Corpos Geniculados , Humanos , Plasticidade Neuronal , Privação Sensorial , TálamoRESUMO
Binocular vision is created by fusing the separate inputs arriving from the left and right eyes. 'Eye dominance' provides a measure of the perceptual dominance of one eye over the other. Theoretical models suggest that eye dominance is related to reciprocal inhibition between monocular units in the primary visual cortex, the first location where the binocular input is combined. As the specific inhibitory interactions in the binocular visual system critically depend on the presence of visual input, we sought to test the role of inhibition by measuring the inhibitory neurotransmitter GABA during monocular visual stimulation of the dominant and the non-dominant eye. GABA levels were measured in a single volume of interest in the early visual cortex, including V1 from both hemispheres, using a combined functional magnetic resonance imaging and magnetic resonance spectroscopy (combined fMRI-MRS) sequence on a 7-Tesla MRI scanner. Individuals with stronger eye dominance had a greater difference in GABAergic inhibition between the eyes. This relationship was present only when the visual system was actively processing sensory input and was not present at rest. We provide the first evidence that imbalances in GABA levels during ongoing sensory processing are related to eye dominance in the human visual cortex. Our finding supports the view that intracortical inhibition underlies normal eye dominance.
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Dominância Ocular/fisiologia , Neurônios GABAérgicos/fisiologia , Inibição Neural/fisiologia , Córtex Visual/fisiologia , Adulto , Feminino , Humanos , Imageamento por Ressonância Magnética , Espectroscopia de Ressonância Magnética , Masculino , Oxigênio/sangue , Estimulação Luminosa , Visão Binocular , Adulto Jovem , Ácido gama-Aminobutírico/metabolismoRESUMO
BACKGROUND/OBJECTIVES: Obesity leads to changes in synaptic plasticity. We aimed at investigating the impact of bariatric surgery (RYGB) on visual neural plasticity (NP) and its relationship with the main gut peptides, leptin, and brain-derived neurotrophic factor (BDNF). SUBJECTS/METHODS: NP was assessed testing binocular rivalry before and after 2 h of monocular deprivation (index of visual brain plasticity) in 15 subjects with obesity (age 42.3 ± 9.8 years; BMI 46.1 ± 4.9 kg/m2) before and after RYGB. Gut peptides, leptin, and BDNF were obtained at baseline and 6 months after surgery in 13 subjects. RESULTS: A significant reduction in BMI (p < 0.001 vs. baseline) and a significant increase of disposition index (DI, p = 0.02 vs baseline) were observed after RYGB. Total and active GLP-1 release in response to glucose ingestion significantly increased after RYGB, while no changes occurred in VIP, GIP, and BDNF levels. Fasting leptin concentration was lower after RYGB (p = 0.001 vs. baseline). Following RYGB, NP was progressively restored (p < 0.002). NP was correlated with DI and fasting glucose at baseline (r = 0.75, p = 0.01; r = -0.7, p = 0.02; respectively), but not with BMI. A positive correlation between post-pre-RYGB changes in AUCactive GLP-1 and NP was observed (r = 0.70, p < 0.01). Leptin was inversely correlated with NP 6 months after surgery (r = -0.63, p = 0.02). No correlation was observed between GIP, VIP, BDNF, and NP. CONCLUSIONS: Visual plasticity is altered in subjects with obesity, and it can be restored after RYGB. The improvement may be mediated by amelioration of insulin sensitivity, increased GLP-1 levels, and reduced leptin levels.
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Cirurgia Bariátrica , Plasticidade Neuronal/fisiologia , Obesidade Mórbida , Córtex Visual/fisiologia , Adolescente , Adulto , Feminino , Humanos , Resistência à Insulina/fisiologia , Masculino , Pessoa de Meia-Idade , Obesidade Mórbida/epidemiologia , Obesidade Mórbida/fisiopatologia , Obesidade Mórbida/cirurgia , Adulto JovemRESUMO
Brain plasticity refers to the ability of synaptic connections to adapt their function and structure in response to experience, including environmental changes, sensory deprivation and injuries. Plasticity is a distinctive, but not exclusive, property of the developing nervous system. This review introduces the concept of neuroplasticity and describes classic paradigms to illustrate cellular and molecular mechanisms underlying synapse modifiability. Then, we summarize a growing number of studies showing that the adult cerebral cortex retains a significant degree of plasticity highlighting how the identification of strategies to enhance the plastic potential of the adult brain could pave the way for the development of novel therapeutic approaches aimed at treating amblyopia and other neurodevelopmental disorders. Finally, we analyze how the visual system adjusts to neurodegenerative conditions leading to blindness and we discuss the crucial role of spared plasticity in the visual system for sight recovery.
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Plasticidade Neuronal/fisiologia , Córtex Visual/fisiologia , Córtex Visual/fisiopatologia , Animais , Humanos , Transtornos da Visão/fisiopatologiaRESUMO
Between 1-5:100 people worldwide have never experienced normotypic vision due to a condition called amblyopia, and about 1:4000 suffer from inherited retinal dystrophies that progressively lead to blindness. While a wide range of technologies and therapies are being developed to restore vision, a fundamental question still remains unanswered: would the adult visual brain retain a sufficient plastic potential to learn how to 'see' after a prolonged period of abnormal visual experience? In this review we summarize studies showing that the visual brain of sighted adults retains a type of developmental plasticity, called homeostatic plasticity, and this property has been recently exploited successfully for adult amblyopia recovery. Next, we discuss how the brain circuits reorganize when blindness occurs and when visual stimulation is partially restored by means of a 'bionic eye' in late blind adults with Retinitis Pigmentosa. The primary visual cortex in these patients slowly became activated by the artificial visual stimulation, indicating that sight restoration therapies can rely on a considerable degree of spared plasticity in adulthood.
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Ambliopia/fisiopatologia , Cegueira/fisiopatologia , Excitabilidade Cortical/fisiologia , Plasticidade Neuronal/fisiologia , Retinose Pigmentar/fisiopatologia , Privação Sensorial/fisiologia , Córtex Visual/fisiologia , Ambliopia/reabilitação , Cegueira/reabilitação , Humanos , Retinose Pigmentar/reabilitação , Córtex Visual/fisiopatologiaRESUMO
Growing evidence indicates a close link between energy metabolism and neural plasticity as obesity is associated with alterations of cognitive functions, memory, and hippocampal neurogenesis. However, it is still unknown whether obesity can affect low-level sensory plasticity. Here we investigated this issue by probing early visual plasticity induced by short-term (2 h) monocular deprivation in a group of adult volunteers with a wide range of Body Mass Index (BMI), from normal weight to morbid obesity. We found that the effect of monocular deprivation decreased with increasing BMI, and morbidly obese subjects (BMI>40) failed to show the homeostatic plasticity effect seen in normal-weight participants. In addition, morbidly obese subjects exhibited altered binocular rivalry dynamics compared with normal-weight observers. These results show for the first time that the impact of obesity observed at the neural and cognitive level extends to basic sensory processing and plasticity.
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Purpose: Retinitis pigmentosa is a family of genetic diseases inducing progressive photoreceptor degeneration. There is no cure for retinitis pigmentosa, but prospective therapeutic strategies are aimed at restoring or substituting retinal input. Yet, it is unclear whether the visual cortex of retinitis pigmentosa patients retains plasticity to react to the restored visual input. Methods: To investigate short-term visual cortical plasticity in retinitis pigmentosa, we tested the effect of short-term (2 hours) monocular deprivation on sensory ocular dominance (measured with binocular rivalry) in a group of 14 patients diagnosed with retinitis pigmentosa with a central visual field sparing greater than 20° in diameter. Results: After deprivation most patients showed a perceptual shift in ocular dominance in favor of the deprived eye (P < 0.001), as did control subjects, indicating a level of visual cortical plasticity in the normal range. The deprivation effect correlated negatively with visual acuity (r = -0.63, P = 0.015), and with the amplitude of the central 18° focal electroretinogram (r = -0.68, P = 0.015) of the deprived eye, revealing that in retinitis pigmentosa stronger visual impairment is associated with higher plasticity. Conclusions: Our results provide a new tool to assess the ability of retinitis pigmentosa patients to adapt to altered visual inputs, and suggest that in retinitis pigmentosa the adult brain has sufficient short-term plasticity to benefit from prospective therapies.
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Plasticidade Neuronal/fisiologia , Retinose Pigmentar/fisiopatologia , Córtex Visual/fisiologia , Adulto , Dominância Ocular/fisiologia , Eletrorretinografia , Feminino , Humanos , Masculino , Pessoa de Meia-Idade , Estudos Prospectivos , Disparidade Visual/fisiologia , Visão Binocular/fisiologia , Acuidade Visual/fisiologia , Campos Visuais/fisiologiaRESUMO
Objectives: The aim of this study was to investigate whether short-term inverse occlusion, combined with moderate physical exercise, could promote the recovery of visual acuity and stereopsis in a group of adult anisometropic amblyopes. Methods: Ten adult anisometropic patients underwent six brief (2 h) training sessions over a period of 4 weeks. Each training session consisted in the occlusion of the amblyopic eye combined with physical exercise (intermittent cycling on a stationary bike). Visual acuity (measured with ETDRS charts), stereoacuity (measured with the TNO test), and sensory eye dominance (measured with binocular rivalry) were tested before and after each training session, as well as in follow-up visits performed 1 month, 3 months, and 1 year after the end of the training. Results: After six brief (2 h) training sessions, visual acuity improved in all 10 patients (0.15 ± 0.02 LogMar), and six of them also recovered stereopsis. The improvement was preserved for up to 1 year after training. A pilot experiment suggested that physical activity might play an important role for the recovery of visual acuity and stereopsis. Conclusions: Our results suggest a noninvasive training strategy for adult human amblyopia based on an inverse-occlusion procedure combined with physical exercise.
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Ambliopia/reabilitação , Dominância Ocular/fisiologia , Privação Sensorial/fisiologia , Visão Binocular/fisiologia , Ambliopia/diagnóstico , Percepção de Profundidade/fisiologia , Exercício Físico/fisiologia , Óculos , Feminino , Humanos , Masculino , Acuidade Visual/fisiologiaRESUMO
Sensory deprivation during the post-natal 'critical period' leads to structural reorganization of the developing visual cortex. In adulthood, the visual cortex retains some flexibility and adapts to sensory deprivation. Here we show that short-term (2 hr) monocular deprivation in adult humans boosts the BOLD response to the deprived eye, changing ocular dominance of V1 vertices, consistent with homeostatic plasticity. The boost is strongest in V1, present in V2, V3 and V4 but absent in V3a and hMT+. Assessment of spatial frequency tuning in V1 by a population Receptive-Field technique shows that deprivation primarily boosts high spatial frequencies, consistent with a primary involvement of the parvocellular pathway. Crucially, the V1 deprivation effect correlates across participants with the perceptual increase of the deprived eye dominance assessed with binocular rivalry, suggesting a common origin. Our results demonstrate that visual cortex, particularly the ventral pathway, retains a high potential for homeostatic plasticity in the human adult.
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Olho/crescimento & desenvolvimento , Plasticidade Neuronal/fisiologia , Privação Sensorial/fisiologia , Córtex Visual/crescimento & desenvolvimento , Adulto , Animais , Dominância Ocular/fisiologia , Feminino , Humanos , Masculino , Visão Binocular/fisiologia , Córtex Visual/fisiologiaRESUMO
[This corrects the article DOI: 10.1155/2017/6724631.].
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When different images are presented to the eyes, the brain is faced with ambiguity, causing perceptual bistability: visual perception continuously alternates between the monocular images, a phenomenon called binocular rivalry. Many models of rivalry suggest that its temporal dynamics depend on mutual inhibition among neurons representing competing images. These models predict that rivalry should be different in autism, which has been proposed to present an atypical ratio of excitation and inhibition [the E/I imbalance hypothesis; Rubenstein & Merzenich, 2003]. In line with this prediction, some recent studies have provided evidence for atypical binocular rivalry dynamics in autistic adults. In this study, we examined if these findings generalize to autistic children. We developed a child-friendly binocular rivalry paradigm, which included two types of stimuli, low- and high-complexity, and compared rivalry dynamics in groups of autistic and age- and intellectual ability-matched typical children. Unexpectedly, the two groups of children presented the same number of perceptual transitions and the same mean phase durations (times perceiving one of the two stimuli). Yet autistic children reported mixed percepts for a shorter proportion of time (a difference which was in the opposite direction to previous adult studies), while elevated autistic symptomatology was associated with shorter mixed perception periods. Rivalry in the two groups was affected similarly by stimulus type, and consistent with previous findings. Our results suggest that rivalry dynamics are differentially affected in adults and developing autistic children and could be accounted for by hierarchical models of binocular rivalry, including both inhibition and top-down influences. Autism Res 2017. ©2017 The Authors Autism Research published by Wiley Periodicals, Inc. on behalf of International Society for Autism Research Autism Res 2017, 10: 1096-1106. © 2017 International Society for Autism Research, Wiley Periodicals, Inc.