Limited restoration of contrast sensitivity with training after V1 damage in humans.

Stroke damage to the primary visual cortex (V1) causes severe visual deficits, which benefit from perceptual retraining. However, whereas training with high-contrast stimuli can locally restore orientation and motion direction discrimination abilities at trained locations, it only partially restores luminance contrast sensitivity (CS). Recent work revealed that high-contrast discrimination abilities may be preserved in the blind field of some patients early after stroke. Here, we asked if CS for orientation and direction discrimination is similarly preserved inside the blind field, to what extent, and whether it could benefit from a visual training intervention. Thirteen subacute patients (<3 months post-V1-stroke) and 12 chronic patients (>6 months post-V1-stroke) were pre-tested, then trained to discriminate either orientation or motion direction of Gabor patches of progressively lower contrasts as their performance improved. At baseline, more subacute than chronic participants could correctly discriminate the orientation of high-contrast Gabors in their blind field, but all failed to perform this task at lower contrasts, even when 10Hz flicker or motion direction were added. Training improved CS in a greater portion of subacute than chronic participants, but no-one attained normal CS, even when stimuli contained flicker or motion. We conclude that, unlike the near-complete training-induced restoration of high-contrast orientation and motion direction discrimination abilities, V1 damage in adulthood may severely limit the residual visual system's ability to regain normal CS. Our results support the notion that CS involves different neural substrates and computations than those required for orientation and direction discrimination in V1-damaged visual systems.Significance statement Stroke-induced V1 damage in adult humans induces a rapid and severe impairment of contrast sensitivity for orientation and motion direction discrimination in the affected hemifield, although discrimination of high-contrast stimuli can persist for several months. Adaptive training with Gabor patches of progressively lower contrasts improves contrast sensitivity for both orientation and motion discriminations in the blind-field of subacute (<3 months post-stroke) and chronic (>6 months post-stroke) participants; however, it fails to restore normal contrast sensitivity. Nonetheless, more subacute than chronic stroke participants benefit from such training, particularly when discriminating the orientation of static, non-flickering targets. Thus, contrast sensitivity appears critically dependent on processing within V1, with perceptual training displaying limited potential to fully restore it after V1 damage.

Contrast sensitivity: a fundamental limit to vision restoration after V1 damage.

Stroke damage to the primary visual cortex (V1) causes severe visual deficits, which benefit from perceptual retraining. However, whereas training with high-contrast stimuli can locally restore orientation and direction discrimination abilities at trained locations, it only partially restores luminance contrast sensitivity (CS). Recent work revealed that high-contrast discrimination abilities may be preserved in the blind field of some patients early after stroke. Here, we asked if CS for orientation and direction discrimination is similarly preserved inside the blind field, to what extent, and whether it could benefit from a visual training intervention. Thirteen subacute (<3 months post-V1-stroke) and 12 chronic (>6 months post-V1-stroke) participants were pre-tested, then trained to discriminate either orientation or motion direction of Gabor patches of progressively lower contrasts. At baseline, more subacute than chronic participants could correctly discriminate the orientation of high-contrast Gabors in their blind field, but all failed to perform this task at lower contrasts, even when 10Hz flicker or motion direction were added. Training improved CS in a greater portion of subacute than chronic participants, but no-one attained normal CS, even when stimuli contained flicker or motion. We conclude that, unlike the near-complete training-induced restoration of high-contrast orientation and direction discrimination, there is limited capacity for restoring CS after V1 damage in adulthood. Our results suggest that CS involves different neural substrates and computations than those required for orientation and direction discrimination in V1-damaged visual systems.

Spared perilesional V1 activity underlies training-induced recovery of luminance detection sensitivity in cortically-blind patients.

Damage to the primary visual cortex (V1) causes homonymous visual-field loss long considered intractable. Multiple studies now show that perceptual training can restore visual functions in chronic cortically-induced blindness (CB). A popular hypothesis is that training can harness residual visual functions by recruiting intact extrageniculostriate pathways. Training may also induce plastic changes within spared regions of the damaged V1. Here, we link changes in luminance detection sensitivity with retinotopic fMRI activity before and after visual discrimination training in eleven patients with chronic, stroke-induced CB. We show that spared V1 activity representing perimetrically-blind locations prior to training predicts the amount of training-induced recovery of luminance detection sensitivity. Additionally, training results in an enlargement of population receptive fields in perilesional V1, which increases blind-field coverage and may support further recovery with subsequent training. These findings uncover fundamental changes in perilesional V1 cortex underlying training-induced restoration of conscious luminance detection sensitivity in CB.

Functional preservation and enhanced capacity for visual restoration in subacute occipital stroke.

Stroke damage to the primary visual cortex (V1) causes a loss of vision known as hemianopia or cortically-induced blindness. While perimetric visual field improvements can occur spontaneously in the first few months post-stroke, by 6 months post-stroke, the deficit is considered chronic and permanent. Despite evidence from sensorimotor stroke showing that early injury responses heighten neuroplastic potential, to date, visual rehabilitation research has focused on patients with chronic cortically-induced blindness. Consequently, little is known about the functional properties of the post-stroke visual system in the subacute period, nor do we know if these properties can be harnessed to enhance visual recovery. Here, for the first time, we show that 'conscious' visual discrimination abilities are often preserved inside subacute, perimetrically-defined blind fields, but they disappear by ∼6 months post-stroke. Complementing this discovery, we now show that training initiated subacutely can recover global motion discrimination and integration, as well as luminance detection perimetry, just as it does in chronic cortically-induced blindness. However, subacute recovery was attained six times faster; it also generalized to deeper, untrained regions of the blind field, and to other (untrained) aspects of motion perception, preventing their degradation upon reaching the chronic period. In contrast, untrained subacutes exhibited spontaneous improvements in luminance detection perimetry, but spontaneous recovery of motion discriminations was never observed. Thus, in cortically-induced blindness, the early post-stroke period appears characterized by gradual-rather than sudden-loss of visual processing. Subacute training stops this degradation, and is far more efficient at eliciting recovery than identical training in the chronic period. Finally, spontaneous visual improvements in subacutes were restricted to luminance detection; discrimination abilities only recovered following deliberate training. Our findings suggest that after V1 damage, rather than waiting for vision to stabilize, early training interventions may be key to maximize the system's potential for recovery.

Spatial suppression promotes rapid figure-ground segmentation of moving objects.

Segregation of objects from their backgrounds is a fundamental visual function and one that is particularly effective when objects are in motion. Theoretically, suppressive center-surround mechanisms are well suited for accomplishing motion segregation. This longstanding hypothesis, however, has received limited empirical support. We report converging correlational and causal evidence that spatial suppression of background motion signals is critical for rapid segmentation of moving objects. Motion segregation ability is strongly predicted by both individual and stimulus-driven variations in spatial suppression strength. Moreover, aging-related superiority in perceiving background motion is associated with profound impairments in motion segregation. This segregation deficit is alleviated via perceptual learning, but only when motion segregation training also causes decreased sensitivity to background motion. We argue that perceptual insensitivity to large moving stimuli effectively implements background subtraction, which, in turn, enhances the visibility of moving objects and accounts for the observed link between spatial suppression and motion segregation.

Boosting Learning Efficacy with Noninvasive Brain Stimulation in Intact and Brain-Damaged Humans.

Numerous behavioral studies have shown that visual function can improve with training, although perceptual refinements generally require weeks to months of training to attain. This, along with questions about long-term retention of learning, limits practical and clinical applications of many such paradigms. Here, we show for the first time in female and male human participants that just 10 d of visual training coupled with transcranial random noise stimulation (tRNS) over visual areas causes dramatic improvements in visual motion perception. Relative to control conditions and anodal stimulation, tRNS-enhanced learning was at least twice as fast, and, crucially, it persisted for 6 months after the end of training and stimulation. Notably, tRNS also boosted learning in patients with chronic cortical blindness, leading to recovery of motion processing in the blind field after just 10 d of training, a period too short to elicit enhancements with training alone. In sum, our results reveal a remarkable enhancement of the capacity for long-lasting plastic and restorative changes when a neuromodulatory intervention is coupled with visual training.SIGNIFICANCE STATEMENT Our work demonstrates that visual training coupled with brain stimulation can dramatically reduce the training period from months to weeks, and lead to fast improvement in neurotypical subjects and chronic cortically blind patients, indicating the potential of our procedure to help restore damaged visual abilities for currently untreatable visual dysfunctions. Together, these results indicate the critical role of early visual areas in perceptual learning and reveal its capacity for long-lasting plastic changes promoted by neuromodulatory intervention.

Perceptual training profoundly alters binocular rivalry through both sensory and attentional enhancements.

The effects of attention, as well as its functional utility, are particularly prominent when selecting among multiple stimuli that compete for processing resources. However, existing studies have found that binocular rivalry-a phenomenon characterized by perceptual competition between incompatible stimuli presented to the two eyes-is only modestly influenced by selective attention. Here, we demonstrate that the relative resistance of binocular rivalry to selective modulations gradually erodes over the course of extended perceptual training that uses a demanding, feature-based attentional task. The final result was a dramatic alteration in binocular rivalry dynamics, leading to profound predominance of the trained stimulus. In some cases, trained observers saw the trained rival image nearly exclusively throughout 4-min viewing periods. This large change in binocular rivalry predominance was driven by two factors: task-independent, eye-specific changes in visual processing, as well as an enhanced ability of attention to promote predominance of the task-relevant stimulus. Notably, this strengthening of task-driven attention also exhibited eye specificity above and beyond that from observed sensory processing changes. These empirical results, along with simulations from a recently developed model of interocular suppression, reveal that stimulus predominance during binocular rivalry can be realized both through an eye-specific boost in processing of sensory information and through facilitated deployment of attention to task-relevant features in the trained eye. Our findings highlight the interplay of attention and binocular rivalry at multiple visual processing stages and reveal that sustained training can substantially alter early visual mechanisms.

Relearning to See in Cortical Blindness.

The incidence of cortically induced blindness is increasing as our population ages. The major cause of cortically induced blindness is stroke affecting the primary visual cortex. While the impact of this form of vision loss is devastating to quality of life, the development of principled, effective rehabilitation strategies for this condition lags far behind those used to treat motor stroke victims. Here we summarize recent developments in the still emerging field of visual restitution therapy, and compare the relative effectiveness of different approaches. We also draw insights into the properties of recovered vision, its limitations and likely neural substrates. We hope that these insights will guide future research and bring us closer to the goal of providing much-needed rehabilitation solutions for this patient population.

Visual recovery in cortical blindness is limited by high internal noise.

Damage to the primary visual cortex typically causes cortical blindness (CB) in the hemifield contralateral to the damaged hemisphere. Recent evidence indicates that visual training can partially reverse CB at trained locations. Whereas training induces near-complete recovery of coarse direction and orientation discriminations, deficits in fine motion processing remain. Here, we systematically disentangle components of the perceptual inefficiencies present in CB fields before and after coarse direction discrimination training. In seven human CB subjects, we measured threshold versus noise functions before and after coarse direction discrimination training in the blind field and at corresponding intact field locations. Threshold versus noise functions were analyzed within the framework of the linear amplifier model and the perceptual template model. Linear amplifier model analysis identified internal noise as a key factor differentiating motion processing across the tested areas, with visual training reducing internal noise in the blind field. Differences in internal noise also explained residual perceptual deficits at retrained locations. These findings were confirmed with perceptual template model analysis, which further revealed that the major residual deficits between retrained and intact field locations could be explained by differences in internal additive noise. There were no significant differences in multiplicative noise or the ability to process external noise. Together, these results highlight the critical role of altered internal noise processing in mediating training-induced visual recovery in CB fields, and may explain residual perceptual deficits relative to intact regions of the visual field.

When can attention influence binocular rivalry?

Attentional influence over perception is particularly pronounced when sensory stimulation is ambiguous, where attention can reduce stimulus uncertainty and promote a stable interpretation of the world. However, binocular rivalry, an extensively studied visual ambiguity, has proved to be comparatively resistant to attentional modulation. We hypothesize that this apparent inconsistency reflects fluctuations in the degree of unresolved competition during binocular rivalry. Namely, attentional influence over rivalry dynamics should be limited to phases of relatively unresolved stimulus competition, such as ends of individual dominance periods. We found that transient, feature-based cues congruent with the dominant stimulus prolonged dominance durations, while cues matching the suppressed stimulus hastened its return to dominance. Notably, the effect of cues depended on when the cues are presented. Cues presented late, but not early, during a given episode of perceptual dominance influenced rivalry dynamics. This temporal pattern mirrors known changes in the relative competitive dynamics of rival stimuli, revealing that selective effects occur only during temporal windows containing weak resolution of visual competition. In conclusion, these findings reveal that unresolved competition, which gates attention across a variety of domains, is also crucial in determining the susceptibility of binocular rivalry to selective influences.

A strong interactive link between sensory discriminations and intelligence.

Early psychologists, including Galton, Cattell, and Spearman, proposed that intelligence and simple sensory discriminations are constrained by common neural processes, predicting a close link between them. However, strong supporting evidence for this hypothesis remains elusive. Although people with higher intelligence quotients (IQs) are quicker at processing sensory stimuli, these broadly replicated findings explain a relatively modest proportion of variance in IQ. Processing speed alone is, arguably, a poor match for the information processing demands on the neural system. Our brains operate on overwhelming amounts of information, and thus their efficiency is fundamentally constrained by an ability to suppress irrelevant information. Here, we show that individual variability in a simple visual discrimination task that reflects both processing speed and perceptual suppression strongly correlates with IQ. High-IQ individuals, although quick at perceiving small moving objects, exhibit disproportionately large impairments in perceiving motion as stimulus size increases. These findings link intelligence with low-level sensory suppression of large moving patterns--background-like stimuli that are ecologically less relevant. We conjecture that the ability to suppress irrelevant and rapidly process relevant information fundamentally constrains both sensory discriminations and intelligence, providing an information-processing basis for the observed link.