Edited by: Olivier A. Coubard, CNS-Fed, France
Reviewed by: Arash Sahraie, University of Aberdeen, UK; Marco Tamietto, Tilburg University, Netherlands
*Correspondence: Sylvie Chokron, Neurology, Unité Fonctionnelle Vision et Cognition, Fondation Ophtalmologique Rothschild, 25, Rue Manin, 75019 Paris, France e-mail:
This article was submitted to the journal Frontiers in Integrative Neuroscience.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Strong evidence of considerable plasticity in primary sensory areas in the adult cortex, and of dramatic cross-modal reorganization in visual areas, after short- or long-term visual deprivation has recently been reported. In the context of patient rehabilitation, this scientifically challenging topic takes on urgent clinical relevance, especially given the lack of information about the role of such reorganization on spared or newly emerged visual performance. Amongst the most common visual field defects found upon unilateral occipital damage of the primary visual cortex is homonymous hemianopia (HH), a perfectly symmetric loss of vision in both eyes. Traditionally, geniculostriate lesions were considered to result in complete and permanent visual loss in the topographically related area of the visual field (Huber,
Although cortical visual impairments (CVI) are frequently encountered after brain damage, they are unfortunately rarely considered in neuro-rehabilitation programs. Whereas traditionally, the treatment of speech, language, and motor disorders is systematic, no visual training is usually proposed to patients with CVI.
The most frequent CVI in brain-damaged patients is homonymous hemianopia (HH), a total loss of vision in the contralesional hemifield of both eyes (Zhang et al.,
Surprisingly, albeit visual-field rehabilitation has been neglected, a growing number of studies on brain-damaged patients have focused on the dissociation between severely impaired explicit (conscious) vision and preserved implicit (unconscious) vision. Indeed, numerous studies in monkeys or humans with retrochiasmatic lesions have shown that some visual functions can be preserved (Humphrey and Weiskrantz,
In the review presented here, we had three objectives. Firstly, we sought to provide an overview of hemianopia and of its deleterious consequences on perception and daily life activities. Secondly, we devised new compensation and restoration techniques to treat visual field defects, emphasizing that remaining unconscious visual capacities are invaluable for restoring the visual field. Finally, we explored the possible cortical mechanisms behind restoration of visual function, by briefly overviewing neuroimaging studies on cortical plasticity in patients that had suffered from visual-field defects.
The loss of vision in HH cannot be explained by injury to the eye itself (Hécaen,
The most frequent etiology of CVI is stroke (either ischemic or hemorrhagic). According to Marshall et al. (
The aforementioned findings are testament to the urgency of visual field rehabilitation in public health. HH and other visual field defects can also result from brain tumors, cerebral hypoxia, along postchiasmatic visual pathways, occipital lobectomies, trauma, progressive multifocal leukoencephalopathy (Diller and Thompson,
In addition to not being able to detect visual stimuli in their contralesional visual field, HH patients suffer from other clinical manifestations, including impaired visual search/orientation in 2D and 3D space, reading difficulties (see below), and slowed and inaccurate performance in functional visual activities (Pambakian et al.,
Although HH patients exhibit partial or complete apparent visual loss in their contralesional visual field in objective perimetric examinations, some of them present unexpected visual capacities in their blind visual field. For example, certain patients can guide one of their hands towards a small line, according to its orientation, even though they claim that they are unaware of the stimulus (Weiskrantz et al.,
Blindsight phenomenon has been observed in numerous tasks. Numerous experiments performed over the past several decades have shown various residual capacities in the blind field of HH patients. Using forced-choice procedures, researchers have highlighted the capacities of these patients to detect a visual stimulus placed in their blind field (Fendrich et al.,
Blindsight was not only reported for simple visual tasks such as grasping but also for tasks requiring more complex visual processing. As a matter of fact, some patients were found to be able to analyse the visual stimulus in order to perform category discrimination (Trevethan et al.,
In a very recent study on hemianopic patients, Fayel et al. (
Blindsight has also been described in children. For instance, Tinelli et al. (
Visual pathways predominantly arise to the primary visual cortex (V1). Considering the global neuronal workspace (GNW) framework (Sergent and Dehaene,
Various hypotheses have been proposed to explain blindsight, including the presence of spared islands in V1 and the projection of visual information from the superior colliculus (SC) or LGN to preserved visual areas. We discuss these mechanisms in the following section.
Given that blindsight is not observed in all hemianopic patients, some researchers have suggested that the residual visual capacities observed in some patients are enabled by spared islands in the primary visual cortex (i.e., areas that retain their function after the lesion) (Fendrich et al.,
The proposed secondary visual pathway would represent an alternative to the major retino-geniculo-striate pathway and entail transfer of visual information to extrastriate cortical areas through the SC or the LGN. The basis for this hypothesis is the principle observation of Riddoch (
Some studies on facial categorization and judgment of facial expressions corroborate the implication of a subcortical pathway. Vuilleumier et al. (
Despite the aforementioned results, in other neuroimaging studies, the authors reported an absence of relationship between blindsight, and activation of subcortical structures. The lack of evidence highlights the limits of conventional fMRI to study blindsight. This might explain why Leh et al. (
More recently, Bridge et al. (
In summary, blindsight might be enabled by retinotectal projections that bypass V1 and could result from connections specific to it. However, its dynamics remain scarcely understood. Recently, Ioannides et al. (
Below we present the spontaneous recovery of HH, and then examine the various rehabilitation techniques that have been proposed to compensate for and/or reduce this related visual-field defect.
Patients can spontaneously recover from HH, but the probability of such recovery is proportional to the time that has elapsed since the lesion occurred. Reported recovery rates range from 7% to 86% (for a review, see: Sabel and Kasten,
Although HH does not seem to be as debilitating as spatial neglect, it can seriously affect daily activities such as driving, walking in crowded areas, crossing the street, and reading. Problems with these and other activities can pose serious problems for recovering HH patients upon their return to work. Given the poor rate of spontaneous recovery in HH, several training programs have been proposed to help patients recover. These programs can be classified into three categories according to their objectives for the visual-field deficit:
An early but now-defunct substitution technique entailed the use of optical aids (e.g., mirrors or Fresnel prisms) to shift visual information from the blind visual field to the central or the ipsilesional, preserved visual field. However, there were only anecdotal reports of the positive effects of this approach; furthermore, such tools were reported to cause diminished acuity, confusion or even diplopia in patients (for a review, see: Pambakian and Kennard,
Currently, compensatory techniques for HH are used principally to enlarge and reinforce visual search, by training patients in oculomotor strategies. Indeed, there are extensive reports that hemianopic patients have difficulties in visual scanning for object detection, as well as in identifying people. These problems can lead to omission of important parts of a scene and consequently, to poor comprehension and to social misunderstanding. Parafoveal visual-field defects also affect reading (
Compensation therapies can be proposed regarding the fact that recovery from a very severe perceptual deficit can be difficult to obtain. Therefore, they typically involve using and modifying the patient’s preserved capacities to sidestep the impairment or render it less disabling. Accordingly, compensation strategies for HH require the use of the ipsilesional hemifield or of the central visual field to compensate for the blind area in the contralesional hemifield.
In classical oculomotor rehabilitation, patients are trained to search for a stimulus projected into their blind hemifield, and then respond to it as quickly as possible. The target can be presented alone or amongst distracters (Zihl and Werth,
Another compensation technique involves a
Finally, other researchers have focused on the reading impairment caused by HH. For instance, Spitzyna et al. (
Although the aim of these compensatory techniques is not to restore
Attempts to enlarge the visual field appear to be a more encouraging way to help hemianopic patients. Unfortunately, as we explained in the previous section, restoration of visual function may seem impossible in HH patients. This might be linked to the fact that, even if a few studies demonstrated in particular condition (see above) that visual experience is possible even in the absence of V1, generally V1 is considered to be crucial for visual consciousness (Weiskrantz et al.,
Thus, recovery of explicit conscious visual detection in the absence of V1 would imply a degree of neural plasticity that is known to be unattainable after a normal rearrangement during the first 3 months post-lesion. Moreover, whether any reorganization that did occur would be powerful enough to activate conscious vision is unknown. However, studies in animals and humans have shown that perceptual learning is possible in hemianopia (i.e., training can improve visual perception) (Fahle and Poggio,
Most of these studies derive from the use of compensatory techniques: the authors found that training HH patients to direct saccades towards the border zone of their blind field could partially increase the size of their visual field (van der Wildt and Bergsma,
A training device named the Lubeck Reaction Perimeter was created by Schmielau (
A completely different approach to that used in the aforementioned devices is one based on that hypothesis that conscious visual detection could be restored by training unconscious visual processing capacities (i.e., blindsight) in hemianopia.
As we mentioned above, some patients can actually perform visual tasks in their impaired hemifield, despite claiming that they cannot see or feel anything (Weiskrantz et al.,
Although blindsight had been extensively studied from the theoretical and experimental perspectives over the past few decades, only in the past 15 years did a few authors begin to hypothesize that blindsight capacities could be improved through training (Sahraie et al.,
Considering that objective improvement has been reported in some studies on blindsight training, and that the use of tasks that are more ecological might help patients to recover, Chokron et al. (
Interestingly, therapies visual or blindsight stimulation in the contralesional visual field are presently being evaluated in children with visual-field defects, consecutive to perinatal asphyxia, or traumatic brain injury (Dutton and Bax,
The possibility of visual-field restoration raises the question of whether some type of cortical reorganization occurs after a unilateral occipital lesion. As we explain below, further neuroimaging studies on patients before and after blindsight stimulation are required in order to understand how vision might be regained.
Plasticity is a fundamental mechanism for the brain to adjust to sensory changes in the surroundings, to improve perception and to recover from damage to the visual system. Studies on neural plasticity have shown that the brain can react to environmental inputs after a lesion, in infants, children and even seniors. Thus, researchers have demonstrated that part of the areas adjacent to a lesion can replace the function of the affected one, as can occur after sensory-motor defects (Liepert et al.,
Studying blindsight enables researchers to determine, in the absence of the primary visual system, whether the spared or recovered visual ability stems from an existing alternative pathway or from newly formed pathway. As described above, Bridge et al. (
Interestingly, in most of the published studies concerned with cortical reorganization in hemianopic patients, the authors did not address the side of the lesion. This issue was tackled by Perez et al. (
The main question when studying brain reorganization after recovery is:
As explained above, various techniques are now available to compensate for damage, or restore vision, in the hemianopic visual field. Regarding the functional basis of these rehabilitation techniques, some studies have suggested that visual training can induce neural modifications in V1 (Furmanski et al.,
Henriksson et al. (
Recently, Plow et al. (
Taken together, the aforementioned studies suggest that visual training in the blind visual field, regardless of whether it is coupled to TMS, can induce cortical reorganization. Nevertheless, more studies are needed in order to standardize these rehabilitation programs as well as to understand the neural bases of recovery. Furthermore, psychophysical studies are required to determine the extent to which the recovered vision in the hemianopic visual field resembles the vision in the ipsilesional field.
Since hemianopia involves impairment in early perceptual processes, recovery from it was once considered impossible. However, recent findings on blindsight offer new perspectives for recovery of visual function in patients with a post-chiasmatic damage. From a theoretical point of view, we still need to understand how training unconscious visual capacities can lead to a restoration of conscious visual capacities. According to the GNW model (Dehaene and Changeux,
Nevertheless, further testing is required in order to confirm the findings that we have summarized here as well as to explain how they help vision recovery. Furthermore, rehabilitation programs should be generalized and standardized in order to facilitate identification of those patients that are the best candidates for treatment and to enable better treatment. Therefore, and as has been proposed for rehabilitation of spatial neglect, we propose that rehabilitation of hemianopia should include a combination of compensatory and restorative techniques tailored to each patient. Indeed, the majority of studies have shown that the use of both types of techniques should help patients to make improvements in everyday life activities.
Future research on blindsight should include neuroimaging studies. One interesting line of research would be to study the link between neural activation and post-training recovery in HH patients. Another interesting study would be to use fMRI to compare HH patients during the acute phase and after training, once they have recovered their field of vision, in order to understand the neural substrates of visual recovery. Finally, researchers should also compare HH patients that have recovered vision to those that have not, in order to determine if the two groups exhibit the same cortical reorganization.
The Guest Associate Editor Olivier A. Coubard declares that, despite having collaborated in the past with authors Céline Perez and Sylvie Chokron, the review process was handled objectively and no conflict of interest exists. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.