Claudia Lunghi

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.

Brief periods of monocular deprivation disrupt ocular balance in human adult visual cortex

Summary Neuroplasticity is a fundamental property of the developing mammalian visual system, with residual potential in adult human cortex [1]. A short period of abnormal visual experience (such as occlusion of one eye) before closure of the critical period has dramatic and permanent neural consequences, reshaping visual cortical organization in favour of the non-deprived eye [2,3]. We used binocular rivalry [4] — a sensitive probe of neural competition — to demonstrate that adult human visual cortex retains a surprisingly high degree of neural plasticity, with important perceptual consequences. We report that 150 minutes of monocular deprivation strongly affects the dynamics of binocular rivalry, unexpectedly causing the deprived eye to prevail in conscious perception twice as much as the non-deprived eye, with significant effects for up to 90 minutes. Apparent contrast of stimuli presented to the deprived eye was also increased, suggesting that the deprivation acts by up-regulation of cortical gain-control mechanisms of the deprived eye. The results suggest that adult visual cortex retains a good deal of plasticity that could be important in reaction to sensory loss.

Touch Interacts with Vision during Binocular Rivalry with a Tight Orientation Tuning

Multisensory integration is a common feature of the mammalian brain that allows it to deal more efficiently with the ambiguity of sensory input by combining complementary signals from several sensory sources. Growing evidence suggests that multisensory interactions can occur as early as primary sensory cortices. Here we present incompatible visual signals (orthogonal gratings) to each eye to create visual competition between monocular inputs in primary visual cortex where binocular combination would normally take place. The incompatibility prevents binocular fusion and triggers an ambiguous perceptual response in which the two images are perceived one at a time in an irregular alternation. One key function of multisensory integration is to minimize perceptual ambiguity by exploiting cross-sensory congruence. We show that a haptic signal matching one of the visual alternatives helps disambiguate visual perception during binocular rivalry by both prolonging the dominance period of the congruent visual stimulus and by shortening its suppression period. Importantly, this interaction is strictly tuned for orientation, with a mismatch as small as 7.5° between visual and haptic orientations sufficient to annul the interaction. These results indicate important conclusions: first, that vision and touch interact at early levels of visual processing where interocular conflicts are first detected and orientation tunings are narrow, and second, that haptic input can influence visual signals outside of visual awareness, bringing a stimulus made invisible by binocular rivalry suppression back to awareness sooner than would occur without congruent haptic input.

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

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.

A cycling lane for brain rewiring

Summary Brain plasticity, defined as the capability of cerebral neurons to change in response to experience, is fundamental for behavioral adaptability, learning, memory, functional development, and neural repair. The visual cortex is a widely used model for studying neuroplasticity and the underlying mechanisms. Plasticity is maximal in early development, within the so-called critical period, while its levels abruptly decline in adulthood [1]. Recent studies, however, have revealed a significant residual plastic potential of the adult visual cortex by showing that, in adult humans, short-term monocular deprivation alters ocular dominance by homeostatically boosting responses to the deprived eye [2–4]. In animal models, a reopening of critical period plasticity in the adult primary visual cortex has been obtained by a variety of environmental manipulations, such as dark exposure, or environmental enrichment, together with its critical component of enhanced physical exercise [5–8]. Among these non-invasive procedures, physical exercise emerges as particularly interesting for its potential of application to clinics, though there has been a lack of experimental evidence available that physical exercise actually promotes visual plasticity in humans. Here we report that short-term homeostatic plasticity of the adult human visual cortex induced by transient monocular deprivation is potently boosted by moderate levels of voluntary physical activity. These findings could have a bearing in orienting future research in the field of physical activity application to clinical research.

Early interaction between vision and touch during binocular rivalry

Multisensory integration is known to occur at high neural levels, but there is also growing evidence that cross-modal signals can be integrated at the first stages of sensory processing. We investigated whether touch specifically affected vision during binocular rivalry, a particular type of visual bistability that engages neural competition in early visual cortices. We found that tactile signals interact with visual signals outside of awareness, when the visual stimulus congruent with the tactile one is perceptually suppressed during binocular rivalry and when the interaction is strictly tuned for matched visuo-tactile spatial frequencies. We also found that voluntary action does not play a leading role in mediating the effect, since the interaction was observed also when tactile stimulation was passively delivered to the finger. However, simultaneous presentation of visual and tactile stimuli is necessary to elicit the interaction, and an asynchronous priming touch stimulus is not affecting the onset of rivalry. These results point to a very early cross-modal interaction site, probably V1. By showing that spatial proximity between visual and tactile stimuli is a necessary condition for the interaction, we also suggest that the two sensory spatial maps are aligned according to retinotopic coordinates, corroborating the hypothesis of a very early interaction between visual and tactile signals during binocular rivalry.

The Complex Interplay Between Multisensory Integration and Perceptual Awareness

The integration of information has been considered a hallmark of human consciousness, as it requires information being globally available via widespread neural interactions. Yet the complex interdependencies between multisensory integration and perceptual awareness, or consciousness, remain to be defined. While perceptual awareness has traditionally been studied in a single sense, in recent years we have witnessed a surge of interest in the role of multisensory integration in perceptual awareness. Based on a recent IMRF symposium on multisensory awareness, this review discusses three key questions from conceptual, methodological and experimental perspectives: (1) What do we study when we study multisensory awareness? (2) What is the relationship between multisensory integration and perceptual awareness? (3) Which experimental approaches are most promising to characterize multisensory awareness? We hope that this review paper will provoke lively discussions, novel experiments, and conceptual considerations to advance our understanding of the multifaceted interplay between multisensory integration and consciousness.

Congruent tactile stimulation reduces the strength of visual suppression during binocular rivalry

Presenting different images to each eye triggers ‘binocular rivalry’ in which one image is visible and the other suppressed, with the visible image alternating every second or so. We previously showed that binocular rivalry between cross-oriented gratings is altered when the fingertip explores a grooved stimulus aligned with one of the rivaling gratings: the matching visual gratings dominance duration was lengthened and its suppression duration shortened. In a more robust test, we here measure visual contrast sensitivity during rivalry dominance and suppression, with and without exploration of the grooved surface, to determine if rivalry suppression strength is modulated by touch. We find that a visual grating undergoes 45% less suppression when observers touch an aligned grating, compared to a cross-oriented one. Touching an aligned grating also improved visual detection thresholds for the ‘invisible’ suppressed grating by 2.4 dB, relative to a vision-only condition. These results show that congruent haptic stimulation prevents a visual stimulus from becoming deeply suppressed in binocular rivalry. Moreover, because congruent touch acted on the phenomenally invisible grating, this visuo-haptic interaction must precede awareness and likely occurs early in visual processing.

The temporal frequency tuning of continuous flash suppression reveals peak suppression at very low frequencies

Continuous flash suppression (CFS) is a psychophysical technique where a rapidly changing Mondrian pattern viewed by one eye suppresses the target in the other eye for several seconds. Despite the widespread use of CFS to study unconscious visual processes, the temporal tuning of CFS suppression is currently unknown. In the present study we used spatiotemporally filtered dynamic noise as masking stimuli to probe the temporal characteristics of CFS. Surprisingly, we find that suppression in CFS peaks very prominently at approximately 1 Hz, well below the rates typically used in CFS studies (10 Hz or more). As well as a strong bias to low temporal frequencies, CFS suppression is greater for high spatial frequencies and increases with increasing masker contrast, indicating involvement of parvocellular/ventral mechanisms in the suppression process. These results are reminiscent of binocular rivalry, and unifies two phenomenon previously thought to require different explanations.