Short-term Monocular Deprivation Research Articles

Daily dose-response from short-term monocular deprivation in adult humans.

Short-term monocular deprivation (MD) shifts sensory eye balance in favour of the previously deprived eye. The effect of MD on eye balance is significant but brief in adult humans. Recently, researchers and clinicians have attempted to implement MD in clinical settings for adults with impaired binocular vision. Although the effect of MD has been studied in detail in single-session protocols, what is not known is whether the effect of MD on eye balance deteriorates after repeated periods of MD (termed 'perceptual deterioration'). An answer to this question is relevant for two reasons. Firstly, the effect of MD (i.e., dose-response) should not decrease with repeated use if MD is to be used therapeutically (e.g., daily for weeks). Second, it bears upon the question of whether the neural basis of the effects of MD and contrast adaptation, a closely related phenomenon, is the same. The sensory change from contrast adaptation depends on recent experience. If the observer has recently experienced the same adaptation multiple times for consecutive days, then the adaptation effect will be smaller because contrast adaptation exhibits perceptual deterioration, so it is of interest to know if the effects of MD follow suit. This study measured the effect of 2-h MD for seven consecutive days on binocular balance of 15 normally sighted adults. We found that the shift in eye balance from MD stayed consistent, showing no signs of deterioration after subjects experienced multiple periods of MD. This finding shows no loss of effectiveness of repeated daily doses of MD if used therapeutically to rebalance binocular vision in otherwise normal individuals. Furthermore, ocular dominance plasticity, which is the basis of the effects of short-term MD, does not seem to share the property of 'perceptual deterioration' with contrast adaptation, suggesting different neural bases for these two related phenomena.

Negligible contribution of adaptation of ocular opponency neurons to the effect of short-term monocular deprivation.

Modeling work on binocular rivalry has described how ocular opponency neurons represent interocular conflict. These neurons have recently been considered to mediate an ocular dominance shift to the eye that has viewed a backward movie for long during which time the other eye is presented with a regular movie. Unlike typical short-term monocular deprivation, the visual inputs are comparable across eyes in that "dichoptic-backward-movie" paradigm. Therefore, it remains unclear whether the ocular opponency neurons are also responsible for the short-term monocular deprivation effect which is prevalently explained by the homeostatic compensation theory. We designed two experiments from distinct perspectives to investigate this question. In Experiment 1, we mitigated the imbalance in the activity of opponency neurons between the two eyes during monocular deprivation by presenting video stimuli alternately. In Experiment 2, we directly evaluated the response of opponency neurons before and after monocular deprivation using SSVEP techniques. Consistent with each other, both experiments failed to provide reliable evidence supporting the involvement of ocular opponency neurons in the short-term monocular deprivation effect. Our results suggest that ocular opponency neurons may not play an essential role in the short-term monocular deprivation effect, potentially due to interference from the homeostatic plasticity mechanism.

The Suppressive Basis of Ocular Dominance Changes Induced by Short-Term Monocular Deprivation in Normal and Amblyopic Adults.

We aimed to study the effect of short-term monocular deprivation on the suppressive interocular interactions in normals and amblyopes by using a dichoptic masking paradigm. Nine adults with anisometropic or mixed amblyopia and 10 control adults participated in our study. The contrast sensitivity in discriminating a target Gabor dichoptically masked was measured before and after 2 hours of monocular deprivation. The mask consisted of bandpass-filtered noise. Both the target and the mask were horizontally oriented at the spatial frequency of 1.31 cpd. Deprivation was achieved using an opaque patch on the amblyopic eye of amblyopes and the dominant eye of controls. Results were similar in both controls and amblyopes. After 2 hours of monocular deprivation, the previously patched eye showed a significant increase in contrast sensitivity under dichoptic masking, which also suggested reduced suppressive effect from the nonpatched eye. Meanwhile, the contrast sensitivity of the nonpatched eye remained almost unchanged under dichoptic masking. We demonstrate that the ocular dominance changes induced by short-term monocular deprivation-namely, the strengthening of the deprived eye's contribution-are associated with the unilateral and asymmetric changes in suppressive interaction. The suppression from the nondeprived eye is reduced after short-term monocular deprivation. This provides a better understanding of how inverse patching (patching of the amblyopic eye) could, by reducing the suppressive drive from the normally sighted (nondeprived) eye, form the basis of a new treatment for the binocular deficit in amblyopia.

Metaplasticity: Dark exposure boosts local excitability and visual plasticity in adult human cortex.

An interlude of dark exposure for about 1 week is known to shift excitatory/inhibitory (E/I) balance of the mammalian visual cortex, promoting plasticity and accelerating visual recovery in animals that have experienced cortical lesions during development. However, the translational impact of our understanding of dark exposure from animal studies to humans remains elusive. Here, we used magnetic resonance spectroscopy as a probe for E/I balance in the primary visual cortex (V1) to determine the effect of 60min of dark exposure, and measured binocular combination as a behavioural assay to assess visual plasticity in 14 normally sighted human adults. To induce neuroplastic changes in the observers, we introduced 60min of monocular deprivation, which is known to temporarily shift sensory eye balance in favour of the previously deprived eye. We report that prior dark exposure for 60 min strengthens local excitability in V1 and boosts visual plasticity in normal adults. However, we show that it does not promote plasticity in amblyopic adults. Nevertheless, our findings are surprising, given the fact that the interlude is very brief. Interestingly, we find that the increased concentration of the excitatory neurotransmitter is not strongly correlated with the enhanced functional plasticity. Instead, the absolute degree of change in its concentration is related to the boost, suggesting that the dichotomy of cortical excitation and inhibition might not explain the physiological basis of plasticity in humans. We present the first evidence that an environmental manipulation that shifts cortical E/I balance can also act as a metaplastic facilitator for visual plasticity in humans. KEY POINTS: A brief interlude (60min) of dark exposure increased the local concentration of glutamine/glutamate but not that of GABA in the visual cortex of adult humans. After dark exposure, the degree of the shift in sensory eye dominance in favour of the previously deprived eye from short-term monocular deprivation was larger than that from only monocular deprivation. The neurochemical and behavioural measures were associated: the magnitude of the shift in the concentration of glutamine/glutamate was correlated with the boost in perceptual plasticity after dark exposure. Surprisingly, the increase in the concentration of glutamine/glutamate was not correlated with the perceptual boost after dark exposure, suggesting that the physiological mechanism of how E/I balance regulates plasticity is not deterministic. In other words, an increased excitation did not unilaterally promote plasticity.

Short-term monocular deprivation in adult humans alters pulvino-cortical functional connectivity measured with resting-state fMRI at ultra-high field

Short-term monocular deprivation in adult humans alters pulvino-cortical functional connectivity measured with resting-state fMRI at ultra-high field

Short-term monocular pattern deprivation reduces the internal additive noise of the visual system.

Previous studies have shown that short-term monocular pattern deprivation can shift perceptual dominance in favor of the deprived eye. However, little is known about the effect of monocular pattern deprivation on contrast sensitivity (CS) and its corresponding mechanisms. Here, contrast sensitivity function (CSF) in the nondominant eye of normal subjects was evaluated before and after 150 min of monocular pattern deprivation. To obtain a CSF with high precision and efficiency before deprivation effect washout, a quick CSF (qCSF) method was used to assess CS over a wide range of spatial frequencies and at two external noise levels. We found that (1) monocular pattern deprivation effectively improved the CS of the deprived eye with larger effect on high spatial frequencies, (2) CS improvement only occurred when external noise was absent and its amount was spatial frequency dependent, and (3) a perceptual template model (PTM) revealed that decreased internal additive noise accounted for the mechanism of the monocular pattern derivation effect. These findings help us better understand the features of short-term monocular pattern deprivation and shed light on the treatment of amblyopia.

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.

Crossmodal plasticity following short-term monocular deprivation

A brief period of monocular deprivation (MD) induces short-term plasticity of the adult visual system. Whether MD elicits neural changes beyond visual processing is yet unclear. Here, we assessed the specific impact of MD on neural correlates of multisensory processes. Neural oscillations associated with visual and audio-visual processing were measured for both the deprived and the non-deprived eye. Results revealed that MD changed neural activities associated with visual and multisensory processes in an eye-specific manner. Selectively for the deprived eye, alpha synchronization was reduced within the first 150 ms of visual processing. Conversely, gamma activity was enhanced in response to audio-visual events only for the non-deprived eye within 100–300 ms after stimulus onset. The analysis of gamma responses to unisensory auditory events revealed that MD elicited a crossmodal upweight for the non-deprived eye. Distributed source modeling suggested that the right parietal cortex played a major role in neural effects induced by MD. Finally, visual and audio-visual processing alterations emerged for the induced component of the neural oscillations, indicating a prominent role of feedback connectivity. Results reveal the causal impact of MD on both unisensory (visual and auditory) and multisensory (audio-visual) processes and, their frequency-specific profiles. These findings support a model in which MD increases excitability to visual events for the deprived eye and audio-visual and auditory input for the non-deprived eye.

Short-term ocular dominance plasticity is not modulated by visual cortex tDCS but increases with length of monocular deprivation

Transcranial direct current stimulation (tDCS) of the occipital lobe may modulate visual cortex neuroplasticity. We assessed the acute effect of visual cortex anodal (a-)tDCS on ocular dominance plasticity induced by short-term monocular deprivation (MD), a well-established technique for inducing homeostatic plasticity in the visual system. In Experiment 1, active or sham visual cortex tDCS was applied during the last 20 min of 2-h MD following a within-subjects design (n = 17). Ocular dominance was measured using two computerized tests. The magnitude of ocular dominance plasticity was unaffected by a-tDCS. In Experiment 2 (n = 9), we investigated whether a ceiling effect of MD was masking the effect of active tDCS. We replicated Experiment 1 but used only 30 min of MD. The magnitude of ocular dominance plasticity was decreased with the shorter intervention, but there was still no effect of active a-tDCS. Within the constraints of our experimental design and a-tDCS parameters, visual cortex a-tDCS did not modulate the homeostatic mechanisms that drive ocular dominance plasticity in participants with normal binocular vision.

Internal neural states influence the short-term effect of monocular deprivation in human adults.

The adult human visual system maintains the ability to be altered by sensory deprivation. What has not been considered is whether the internal neural states modulate visual sensitivity to short-term monocular deprivation. In this study we manipulated the internal neural state and reported changes in intrinsic neural oscillations with a patched eye open or closed. We investigated the influence of eye open/eye closure on the unpatched eye's contrast sensitivity and ocular dominance (OD) shifts induced by short-term monocular deprivation. The results demonstrate that internal neural states influence not only baseline contrast sensitivity but also the extent to which the adult visual system can undergo changes in ocular dominance.

Effect of fasting on short-term visual plasticity in adult humans.

Brain plasticity and function is impaired in conditions of metabolic dysregulation, such as obesity. Less is known on whether brain function is also affected by transient and physiological metabolic changes, such as the alternation between fasting and fed state. Here we asked whether these changes affect the transient shift of ocular dominance that follows short-term monocular deprivation, a form of homeostatic plasticity. We further asked whether variations in three of the main metabolic and hormonal pathways affected in obesity (glucose metabolism, leptin signalling and fatty acid metabolism) correlate with plasticity changes. We measured the effects of 2 h monocular deprivation in three conditions: post-absorptive state (fasting), after ingestion of a standardised meal and during infusion of glucagon-like peptide-1 (GLP-1), an incretin physiologically released upon meal ingestion that plays a key role in glucose metabolism. We found that short-term plasticity was less manifest in fasting than in fed state, whereas GLP-1 infusion did not elicit reliable changes compared to fasting. Although we confirmed a positive association between plasticity and supraphysiological GLP-1 levels, achieved by GLP-1 infusion, we found that none of the parameters linked to glucose metabolism could predict the plasticity reduction in the fasting versus fed state. Instead, this was selectively associated with the increase in plasma beta-hydroxybutyrate (B-OH) levels during fasting, which suggests a link between neural function and energy substrates alternative to glucose. These results reveal a previously unexplored link between homeostatic brain plasticity and the physiological changes associated with the daily fast-fed cycle.

Short-Term Monocular Deprivation in Adult Humans Alters Functional Brain Connectivity Measured With Ultra-High Field Magnetic Resonance Imaging

Short-Term Monocular Deprivation in Adult Humans Alters Functional Brain Connectivity Measured With Ultra-High Field Magnetic Resonance Imaging

The shift in sensory eye dominance from short-term monocular deprivation exhibits no dependence on test spatial frequency

BackgroundStudies have shown that short-term monocular deprivation induces a shift in sensory eye dominance in favor of the deprived eye. Yet, how short-term monocular deprivation modulates sensory eye dominance across spatial frequency is not clear. To address this issue, we conducted a study to investigate the dependence of short-term monocular deprivation effect on test spatial frequency.MethodsTen healthy young adults (age: 24.7 ± 1.7 years, four males) with normal vision participated. We deprived their dominant eye with a translucent patch for 2.5 h. The interocular contrast ratio (dominant eye/non-dominant eye, i.e., the balance point [BP]), which indicates the contribution that the two eyes make to binocular combination, was measured using a binocular orientation combination task. We assessed if BPs at 0.5, 4 or 6 cycles/degree (c/d) change as a result of monocular deprivation. Different test spatial frequency conditions were conducted on three separate days in a random fashion.ResultsWe compared the BPs at 0.5, 4 and 6 c/d before and after monocular deprivation. The BPs were found to be significantly affected by deprivation, where sensory eye dominance shift to the deprived eye (F1.86, 16.76 = 33.09, P < 0.001). The changes of BP were consistent at 0.5, 4, and 6 c/d spatial frequencies (F2,18 = 0.15, P = 0.57).ConclusionThe sensory eye dominance plasticity induced by short-term deprivation is not dependent on test spatial frequency, suggesting it could provide a practical solution for amblyopic therapy that was concerned with the binocular outcome.

Issues Revisited: Shifts in Binocular Balance Depend on the Deprivation Duration in Normal and Amblyopic Adults.

Recent studies indicate that short-term monocular deprivation increases the deprived eye's contribution to binocular fusion in both adults with normal vision and amblyopia. In this study, we investigated whether the changes in visual plasticity depended on the duration of deprivation in normal and amblyopic adults. Twelve anisometropia amblyopic observers (aged 24.8 ± 2.3years) and 12 age-matched normal observers (aged 23.9 ± 1.2years) participated in the study. The non-dominant eye of normal observers or amblyopic eye of amblyopic observers was deprived for 30, 120, and 300min in a randomized order. Their eye balance was measured with a phase combination task, which is a psychophysical test, before and after the deprivation. This design enabled us to measure changes induced in binocular balance as an index visual plasticity due to monocular deprivations. By comparingthe ocular dominance changes as a result of monocular deprivation with different deprivation durations, we found evidence that the ocular dominance changes are slightly larger after longer deprivations in both normal and amblyopic observers, albeit with a statistical significance. The changesfrom 120-min were significantly greaterthan thosefrom 30-min deprivation in both groups. The magnitude of changes in sensory eye balance was significantly larger in normal observers than that in the amblyopic observers; however, the longevity of changes in visual plasticity was found to be more long-lasting in amblyopic observers than the normal counterparts. The duration of deprivation matters in both normal and amblyopic observers. Ocular dominance imbalance that is typically observed in amblyopia canbe more ameliorated with alonger duration of deprivation.

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.

A brief light reduction induces a significant delay in the previously dimmed eye.

We investigated how a short-term luminance reduction in one eye can influence temporal processing of that eye after luminance is restored by measuring the relative delay between the eyes. A paradigm based on the Pulfrich effect, which is a visual illusion of depth when no depth cue is present, was used to measure relative delay in visual processing between the eyes. We deprived the monocular luminance in adults with normal vision across different intensities. In the first experiment, the ratio of the light level between the eyes stayed constant, whereas the absolute value was allowed to vary. In the second experiment, both the ratio and the absolute light level stayed constant, by controlling the environmental light level. In both experiments, we measured the changes in relative delay before and after 60 min of light deprivation. Our results indicated that short-term monocular deprivation of luminance slows the processing in the previously dimmed eye and that the magnitude of the delay is correlated with the degree of luminance reduction. In addition, we observed that the absolute luminance difference, rather than the absolute luminance levels seen by the dimmed eye, is important in determining the magnitude of delay in the previously dimmed eye. These findings differ from what has been reported previously for the monocular deprivation of contrast. Taken together, these findings support the view that short-term deprivation of visual information could affect two distinct mechanisms (contrast gain and temporal dynamics) of neural plasticity.

The Mechanism of Short-Term Monocular Pattern Deprivation-Induced Perceptual Eye Dominance Plasticity.

Previously published studies have reported that 150 min of short-term monocular deprivation temporarily changes perceptual eye dominance. However, the possible mechanisms underlying monocular deprivation-induced perceptual eye dominance plasticity remain unclear. Using a binocular phase and contrast co-measurement task and a multi-pathway contrast-gain control model (MCM), we studied the effect of 150 min of monocular pattern deprivation (MPD) in normal adult subjects. The perceived phase and contrast varied significantly with the interocular contrast ratio, and after MPD, the patched eye (PE) became dominant. Most importantly, we focused on the potential mechanisms of the deprivation effect. The data of an averaged subject was best fitted by a model, which assumed a monocular signal enhancement of the PE after the MPD. The present findings might have important implications for investigations of binocular vision in both normal and amblyopic populations.

Rapid alternate monocular deprivation does not affect binocular balance and correlation in human adults.

Recent studies show that the human adult visual system exhibits neural plasticity. For instance, short-term monocular deprivation shifts the eye dominance in favor of the deprived eye. This phenomenon is believed to occur in the primary visual cortex by reinstating neural plasticity. However, it is unknown whether the changes in eye dominance after monocularly depriving the visual input can also be induced by alternately depriving both eyes. In this study, we found no changes in binocular balance and interocular correlation sensitivity after a rapid (7 Hz), alternate, and monocular deprivation for 1 h in adults. Therefore, the effect of short-term monocular deprivation cannot seem to be emulated by alternately and rapidly depriving both eyes.

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.

Invited Session III: Reawakening plasticity in visual cortex: Reactivating visual plasticity in adult humans

Neuroplasticity is a fundamental property of the nervous system that is maximal early in life, within a specific temporal window called critical period. However, it is still unclear to which extent the plastic potential of the visual cortex is retained in adulthood. We have surprisingly revealed residual ocular dominance plasticity in adult humans by showing that short-term monocular deprivation unexpectedly boosts the deprived eye (both at the perceptual and at the neural level), reflecting homeostatic plasticity. This effect is accompanied by a decrease of GABAergic inhibition in the primary visual cortex and can be modulated by non-visual factors (physical exercise, motor plasticity and energy metabolism). Finally, we have found that combining short-term reverse occlusion with physical exercise promotes the long-term improvement in visual acuity and stereopsis in adult amblyopic patients. Taken together, these results challenge the classical view of a hard-wired adult visual cortex, indicating that homeostatic plasticity can be reactivated in adult humans.