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.

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.

Role of inter-hemispheric transfer in generating visual evoked potentials in V1-damaged brain hemispheres.

Partial cortical blindness is a visual deficit caused by unilateral damage to the primary visual cortex, a condition previously considered beyond hopes of rehabilitation. However, recent data demonstrate that patients may recover both simple and global motion discrimination following intensive training in their blind field. The present experiments characterized motion-induced neural activity of cortically blind (CB) subjects prior to the onset of visual rehabilitation. This was done to provide information about visual processing capabilities available to mediate training-induced visual improvements. Visual Evoked Potentials (VEPs) were recorded from two experimental groups consisting of 9 CB subjects and 9 age-matched, visually-intact controls. VEPs were collected following lateralized stimulus presentation to each of the 4 visual field quadrants. VEP waveforms were examined for both stimulus-onset (SO) and motion-onset (MO) related components in postero-lateral electrodes. While stimulus presentation to intact regions of the visual field elicited normal SO-P1, SO-N1, SO-P2 and MO-N2 amplitudes and latencies in contralateral brain regions of CB subjects, these components were not observed contralateral to stimulus presentation in blind quadrants of the visual field. In damaged brain hemispheres, SO-VEPs were only recorded following stimulus presentation to intact visual field quadrants, via inter-hemispheric transfer. MO-VEPs were only recorded from damaged left brain hemispheres, possibly reflecting a native left/right asymmetry in inter-hemispheric connections. The present findings suggest that damaged brain hemispheres contain areas capable of responding to visual stimulation. However, in the absence of training or rehabilitation, these areas only generate detectable VEPs in response to stimulation of the intact hemifield of vision.

Beyond blindsight: properties of visual relearning in cortically blind fields.

Damage to the primary visual cortex (V1) or its immediate afferents results in a dense scotoma, termed cortical blindness (CB). CB subjects have residual visual abilities, or blindsight, which allow them to detect and sometimes discriminate stimuli with high temporal and low spatial frequency content. Recent work showed that with training, discriminations in the blind field can become more reliable, and even reach consciousness. However, the narrow spatiotemporal bandwidth of blindsight limits its functional usefulness in everyday vision. Here, we asked whether visual training can induce recovery outside the spatiotemporal bandwidth of blindsight. Specifically, could human CB subjects learn to discriminate static, nonflickering stimuli? Can such learning transfer to untrained stimuli and tasks, and does double training with moving and static stimuli provide additional advantages relative to static training alone? We found CB subjects capable of relearning static orientation discriminations following single as well as double training. However, double training with complex, moving stimuli in a separate location was necessary to recover complex motion thresholds at locations trained with static stimuli. Subjects trained on static stimuli alone could only discriminate simple motion. Finally, both groups had approximately equivalent, incomplete recovery of fine orientation and direction discrimination thresholds, as well as contrast sensitivity. These results support two conclusions: (1) from a practical perspective, complex moving stimuli and double training may be superior training tools for inducing visual recovery in CB, and (2) the cortically blind visual system can relearn to perform a wider range of visual discriminations than predicted by blindsight alone.

Visual cortical activity reflects faster accumulation of information from cortically blind fields.

Brain responses (from functional magnetic resonance imaging) and components of information processing were investigated in nine cortically blind observers performing a global direction discrimination task. Three of these subjects had responses in perilesional cortex in response to blind field stimulation, whereas the others did not. We used the EZ-diffusion model of decision making to understand how cortically blind subjects make a perceptual decision on stimuli presented within their blind field. We found that these subjects had slower accumulation of information in their blind fields as compared with their good fields and to intact controls. Within cortically blind subjects, activity in perilesional tissue, V3A and hMT+ was associated with a faster accumulation of information for deciding direction of motion of stimuli presented in the blind field. This result suggests that the rate of information accumulation is a critical factor in the degree of impairment in cortical blindness and varies greatly among affected individuals. Retraining paradigms that seek to restore visual functions might benefit from focusing on increasing the rate of information accumulation.

Different properties of visual relearning after damage to early versus higher-level visual cortical areas.

The manipulation of visual perceptual learning is emerging as an important rehabilitation tool following visual system damage. Specificity of visual learning for training stimulus and task attributes has been used in prior work to infer a differential contribution of higher-level versus lower-level visual cortical areas to this process. The present study used a controlled experimental paradigm in felines to examine whether relearning of motion discrimination and the specificity of such relearning are differently influenced by damage at lower versus higher levels of the visual cortical hierarchy. Cats with damage to either early visual areas 17,18, and 19, or to higher-level, motion-processing lateral suprasylvian (LS) cortex were trained to perform visual tasks with controlled fixation. Animals with either type of lesion could relearn to discriminate the direction of motion of both drifting gratings and random dot stimuli in their impaired visual field. However, two factors emerged as critical for allowing transfer of learning to untrained motion stimuli: (1) an intact LS cortex and (2) more complex visual stimuli. Thus, while the hierarchical level of visual cortex damage did not seem to limit the ability to relearn motion discriminations, generalizability of relearning with a damaged visual system appeared to be influenced by both the areas damaged and the nature of the stimulus used during training.

New approaches to visual rehabilitation for cortical blindness: outcomes and putative mechanisms.

Cortical blindness is a chronic loss of vision following damage to the primary visual cortex (V1) or its postchiasmal afferents. Such damage is followed by a brief period of spontaneous plasticity that rarely lasts beyond 6 months. Following this initial phase, the visual deficit is thought to be stable, intractable, and permanent. Cortically blind subjects demonstrate spontaneous oculomotor adaptations to their deficits that can be further improved by saccadic localization training. However, saccadic training does not improve visual sensitivity in the blind field. In contrast, recent studies by a number of independent groups suggest that localized, repetitive perceptual training can improve visual sensitivity in the blind field, although mechanisms underlying the observed recovery remain unclear. This review discusses the current literature on rehabilitative strategies used for cortical blindness with emphasis on the use of perceptual training methods. The putative mechanisms that underlie the resulting, training-induced visual improvements are then outlined, along with the special challenges posed to their elucidation by the great variability in the extent and sometimes nature of the V1 damage sustained in different individuals.