Learning to discriminate the eye-of-origin during continuous flash suppression.

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.

Measuring the reliability of binocular rivalry.

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.

Bariatric surgery restores visual cortical plasticity in nondiabetic subjects with obesity.

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.

Early Cross-modal Plasticity in Adults.

It is known that, after a prolonged period of visual deprivation, the adult visual cortex can be recruited for nonvisual processing, reflecting cross-modal plasticity. Here, we investigated whether cross-modal plasticity can occur at short timescales in the typical adult brain by comparing the interaction between vision and touch during binocular rivalry before and after a brief period of monocular deprivation, which strongly alters ocular balance favoring the deprived eye. While viewing dichoptically two gratings of orthogonal orientation, participants were asked to actively explore a haptic grating congruent in orientation to one of the two rivalrous stimuli. We repeated this procedure before and after 150 min of monocular deprivation. We first confirmed that haptic stimulation interacted with vision during rivalry promoting dominance of the congruent visuo-haptic stimulus and that monocular deprivation increased the deprived eye and decreased the nondeprived eye dominance. Interestingly, after deprivation, we found that the effect of touch did not change for the nondeprived eye, whereas it disappeared for the deprived eye, which was potentiated after deprivation. The absence of visuo-haptic interaction for the deprived eye lasted for over 1 hr and was not attributable to a masking induced by the stronger response of the deprived eye as confirmed by a control experiment. Taken together, our results demonstrate that the adult human visual cortex retains a high degree of cross-modal plasticity, which can occur even at very short timescales.

Short-Term Monocular Deprivation Enhances Physiological Pupillary Oscillations.

Short-term monocular deprivation alters visual perception in adult humans, increasing the dominance of the deprived eye, for example, as measured with binocular rivalry. This form of plasticity may depend upon the inhibition/excitation balance in the visual cortex. Recent work suggests that cortical excitability is reliably tracked by dilations and constrictions of the pupils of the eyes. Here, we ask whether monocular deprivation produces a systematic change of pupil behavior, as measured at rest, that is independent of the change of visual perception. During periods of minimal sensory stimulation (in the dark) and task requirements (minimizing body and gaze movements), slow pupil oscillations, "hippus," spontaneously appear. We find that hippus amplitude increases after monocular deprivation, with larger hippus changes in participants showing larger ocular dominance changes (measured by binocular rivalry). This tight correlation suggests that a single latent variable explains both the change of ocular dominance and hippus. We speculate that the neurotransmitter norepinephrine may be implicated in this phenomenon, given its important role in both plasticity and pupil control. On the practical side, our results indicate that measuring the pupil hippus (a simple and short procedure) provides a sensitive index of the change of ocular dominance induced by short-term monocular deprivation, hence a proxy for plasticity.

Corrigendum to "Short-Term Monocular Deprivation Enhances Physiological Pupillary Oscillations".

[This corrects the article DOI: 10.1155/2017/6724631.].

Auditory and tactile signals combine to influence vision during binocular rivalry.

Resolution of perceptual ambiguity is one function of cross-modal interactions. Here we investigate whether auditory and tactile stimuli can influence binocular rivalry generated by interocular temporal conflict in human subjects. Using dichoptic visual stimuli modulating at different temporal frequencies, we added modulating sounds or vibrations congruent with one or the other visual temporal frequency. Auditory and tactile stimulation both interacted with binocular rivalry by promoting dominance of the congruent visual stimulus. This effect depended on the cross-modal modulation strength and was absent when modulation depth declined to 33%. However, when auditory and tactile stimuli that were too weak on their own to bias binocular rivalry were combined, their influence over vision was very strong, suggesting the auditory and tactile temporal signals combined to influence vision. Similarly, interleaving discrete pulses of auditory and tactile stimuli also promoted dominance of the visual stimulus congruent with the supramodal frequency. When auditory and tactile stimuli were presented at maximum strength, but in antiphase, they had no influence over vision for low temporal frequencies, a null effect again suggesting audio-tactile combination. We also found that the cross-modal interaction was frequency-sensitive at low temporal frequencies, when information about temporal phase alignment can be perceptually tracked. These results show that auditory and tactile temporal processing is functionally linked, suggesting a common neural substrate for the two sensory modalities and that at low temporal frequencies visual activity can be synchronized by a congruent cross-modal signal in a frequency-selective way, suggesting the existence of a supramodal temporal binding mechanism.

Short-term monocular deprivation alters early components of visual evoked potentials.

KEY POINTS: Short-term monocular deprivation in adult humans produces a perceptual boost of the deprived eye reflecting homeostatic plasticity. Visual evoked potentials (VEPs) to transient stimuli change after 150 min of monocular deprivation in adult humans. The amplitude of the C1 component of the VEP at a latency of about 100 ms increases for the deprived eye and decreases for the non-deprived eye after deprivation, the two effects being highly negatively correlated. Similarly, the evoked alpha rhythm increases after deprivation for the deprived eye and decreases for the non-deprived eye. The data demonstrate that primary visual cortex excitability is altered by a short period of monocular deprivation, reflecting homeostatic plasticity. ABSTRACT: Very little is known about plasticity in the adult visual cortex. In recent years psychophysical studies have shown that short-term monocular deprivation alters visual perception in adult humans. Specifically, after 150 min of monocular deprivation the deprived eye strongly dominates the dynamics of binocular rivalry, reflecting homeostatic plasticity. Here we investigate the neural mechanisms underlying this form of short-term visual cortical plasticity by measuring visual evoked potentials (VEPs) on the scalp of adult humans during monocular stimulation before and after 150 min of monocular deprivation. We found that monocular deprivation had opposite effects on the amplitude of the earliest component of the VEP (C1) for the deprived and non-deprived eye stimulation. C1 amplitude increased (+66%) for the deprived eye, while it decreased (-29%) for the non-deprived eye. Source localization analysis confirmed that the C1 originates in the primary visual cortex. We further report that following monocular deprivation, the amplitude of the peak of the evoked alpha spectrum increased on average by 23% for the deprived eye and decreased on average by 10% for the non-deprived eye, indicating a change in cortical excitability. These results indicate that a brief period of monocular deprivation alters interocular balance in the primary visual cortex of adult humans by both boosting the activity of the deprived eye and reducing the activity of the non-deprived eye. This indicates a high level of residual homeostatic plasticity in the adult human primary visual cortex, probably mediated by a change in cortical excitability.

Long-term effects of monocular deprivation revealed with binocular rivalry gratings modulated in luminance and in color.

During development, within a specific temporal window called the critical period, the mammalian visual cortex is highly plastic and literally shaped by visual experience; to what extent this extraordinary plasticity is retained in the adult brain is still a debated issue. We tested the residual plastic potential of the adult visual cortex for both achromatic and chromatic vision by measuring binocular rivalry in adult humans following 150 minutes of monocular patching. Paradoxically, monocular deprivation resulted in lengthening of the mean phase duration of both luminance-modulated and equiluminant stimuli for the deprived eye and complementary shortening of nondeprived phase durations, suggesting an initial homeostatic compensation for the lack of information following monocular deprivation. When equiluminant gratings were tested, the effect was measurable for at least 180 minutes after reexposure to binocular vision, compared with 90 minutes for achromatic gratings. Our results suggest that chromatic vision shows a high degree of plasticity, retaining the effect for a duration (180 minutes) longer than that of the deprivation period (150 minutes) and twice as long as that found with achromatic gratings. The results are in line with evidence showing a higher vulnerability of the P pathway to the effects of visual deprivation during development and a slower development of chromatic vision in humans.

Learned value modulates the access to visual awareness during continuous flash suppression.

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.

Different Forms of Plasticity Interact in Adult Humans.

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.

The duration effect of short-term monocular deprivation measured by binocular rivalry and binocular combination.

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.

Attention cueing in rivalry: insights from pupillometry.

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.

Moderate physical activity alters the estimation of time, but not space.

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.

Mutual interaction between visual homeostatic plasticity and sleep in adult humans.

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.

Short-term plasticity in the human visual thalamus.

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.

Neuroplasticity of the visual cortex: in sickness and in health.

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.

GABAergic inhibition in the human visual cortex relates to eye dominance.

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.

Neuroplasticity in adult human visual cortex.

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.

Altered Visual Plasticity in Morbidly Obese Subjects.

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.