Pambakian, Alidz MRCP; Currie, Jon MBBS, PhD; Kennard, Christopher PhD, FRCP, F Med Sci
Homonymous visual field defects (HVFDs) are among the most frequent consequences of brain damage. Thirty percent of all patients with stroke (1) and 70% of those with stroke involving the posterior cerebral artery have hemianopias (2). Subarachnoid hemorrhages, intracerebral hematomas, and trauma add to this figure (3,4). Patients with HVFDs have particular difficulties with reading and visual exploration that have far-reaching repercussions on their domestic and vocational lives (3,4). In addition, HVFDs are associated with a reduced prognosis for successful rehabilitation from stroke (5-8), particularly when combined with visual neglect or visual sensory inattention (9-12). This article updates a previous review of rehabilitation strategies for patients with HVFDs (1). The topic has also been comprehensively reviewed by Kerkhoff (3) and Zihl (4).
Although rehabilitation strategies for aphasia, motor dysfunction, and cognitive dysfunction are widely used in clinical practice, there are no uniformly accepted treatments for HVFDs, and surprisingly little systematic, evidence-based research in this area. As a result, therapeutic nihilism is often the response to rehabilitation of patients with such problems. However, a number of clinical observations should raise optimism regarding the potential for success with a variety of techniques.
PRINCIPLES UNDERLYING VISUAL REHABILITATION
Visual rehabilitation of patients with HVFDs rests on certain physiologic principles and observations.
First, the traditional view that lesions of the geniculostriate pathway in humans result in complete and permanent visual loss in the topographically related area of visual field has been challenged as it has become clear that the “blind” hemifields of hemianopes may retain certain visual functions (13).
Second, some patients eventually experience varying degrees of spontaneous recovery of their visual defect, depending on the underlying pathology and location of the causative lesion (14,15). Studies using 18-fluoro-2-deoxyglucose positron emission tomography have demonstrated a reduction in the size of the metabolic lesion and improvement in striate cortex metabolism in patients with reversible homonymous field defects, but not in patients with persisting field defects (16). HVFDs caused by ischemia show recovery of full visual field in fewer than 10% of cases (5,17). In patients with complete homonymous hemianopias caused by ischemia, field recovery is largely complete within the first 10 days. Recovery of a partial defect is usually maximal within the first 48 hours and complete within 10 to 12 weeks (5,17). In general, vision returns to the affected field in a sequence starting with perception of light, motion, form, color, and finally stereognosis (5,17). Functional brain reorganization may allow recovery of function after the resolution of peri-infarct edema and reperfusion of the ischemic penumbra. However, the strict unilateral retinotopic representation of the primary visual cortex probably limits the degree of reorganization that has been observed in other neural networks that are organized in a more extended and overlapping fashion (18-20).
Third, patients with established HVFDs perform maneuvers designed to compensate for their visual loss. When viewing simple patterns, hemianopic patients concentrate their gaze towards the blind hemifield rather than toward the center of the pattern, demonstrating what is thought by some to be a compensatory strategy (21-23). By deviating their fixation point into the blind field, more of the visual scene is brought into the intact hemifield. They also adopt a number of compensatory strategies when refixating between simple visual targets presented unpredictably (1,24). When performing visual search tasks, patients with long-standing hemianopias scan very differently than do normal subjects and demonstrate numerous refixations and inaccurate saccades that result in disorganized scanning, longer search times, and the omission of relevant objects (22,25). In a recent study, we recorded the eye movements of patients with HVFDs while they viewed images of real scenes (26) and found that those with lesions of less than 6 months' duration made patterns of fixations that approximated those of normal subjects, whereas those with older lesions demonstrated fixation patterns different from those of normal subjects. This finding may reflect the evolution of a spontaneous compensatory eye movement strategy and raises the interesting question of whether patients can be taught to scan more efficiently (25,27-30).
Rehabilitation of patients with HVFDs is based on maximizing whatever visual function remains. Two approaches have been used: optical aids and visual training.
Many optical aids have been promoted but never subjected to clinical trial in the treatment of patients with HVFDs (31-33). These include mirrors attached to spectacle frames (34), partially reflecting mirrors (beam splitters), and dichroic mirrors (which reflect a red image and transmit a green one) (35), reversed telescopes (36), prisms, wide-angle lenses, and closed-circuit television monitors (37).
Optical aids function in one of two ways: (1) to relocate the image to a part of the visual field not within the scotoma; or (2) to expand the visual field. Relocation replaces one scotoma with another, because the relocated image causes another previously visible part of the visual field to become invisible. Field expansion is therefore the preferable option. This has been performed most successfully with prisms.
Prisms have been applied to spectacle lenses to treat HVFDs for more than 30 years with varying anecdotal success. Fresnel prisms work by displacing the images of objects toward their apex and are commercially available as plastic press-on lenses that can easily be applied to spectacle lenses with their bases toward the hemianopic side. Binocular sectoral prisms applied to the hemianopic half of each lens appear to be the most commonly used (38,39). They relocate the image when the patient looks sideways through the prism but cause a scotoma in the primary gaze position. Their use in HVFDs in one controlled trial (38) concluded that the prism-treated group performed significantly better on visuospatial tests but did not demonstrate any functional improvement in activities of daily living. Monocularly fitted sectoral prisms serve to expand the field but cause unacceptable central diplopia (40), which may be overcome by trimming the central area (41). Because of these drawbacks, Fresnel prisms used in this way have never really entered clinical practice. However, two recent modifications offer promise: vision multiplexing and prism adaptation.
Multiplexing refers to the transmission of two or more signals simultaneously over the same communication channel so that all the information can be separated and used at the receiving end. Vision multiplexing is the general engineering approach used by Peli (31,32) to develop a range of visual aids. Under normal circumstances, the visual system allows a wide field of view of almost 180° at very high resolution, which is achieved by using “temporal multiplexing” and variable spatial resolution (33). The peripheral visual fields are continually monitored at low spatial resolution for targets of interest, which are then fixated by the high-resolution fovea via saccadic eye movements. In this way, high-resolution information from several targets of interest is temporally multiplexed and used to generate a high-resolution view over a wide field, even though at any instant only a fraction of the field is seen at such high resolution.
Any visual disorder, such as hemianopia, disrupts the interplay between central and peripheral vision and interrupts multiplexing. A visual multiplexing aid would aim to multiplex the missing component with the remaining one. For hemianopia, the missing peripheral field should be multiplexed with the remaining high-resolution central field in such a way that the visual system can access and interpret both.
An ideal optical aid for patients with HVFDs would therefore: (1) expand the visual field rather than relocate it; (2) function in all positions of gaze; (3) avoid central diplopia; and (4) reconstruct the interplay of central and peripheral vision. Peli (31-33) has developed a visual aid that uses monocular sectoral prisms that are restricted to the peripheral fields (superior, inferior, or both). The prisms are placed across the whole width of the spectacle lens on the side of the hemianopia, above and below the pupil, and provide peripheral field information that is effective in all lateral positions of gaze. The prism expands the field by causing peripheral diplopia, which is a common feature of normal vision and is therefore tolerated far better than central diplopia. The effect is to cause an artificial exotropia in peripheral but not central vision, which is reminiscent of the exotropia that some congenital hemianopes develop as a natural compensatory mechanism (42). A visual field expansion of approximately 20° measurable by standard perimetry has been described in the first 30 patients treated with a 40-diopter prism by Peli (32). Patients have reported improved walking and avoidance of obstacles and appear to accurately perceive the location of objects detected using the device. No formal testing has been conducted, but such an engineering approach offers considerable prospects.
Binocular prisms, fitted the full width of the spectacle lens, function to relocate the whole field of view (43). A 20-diopter prism, for example, shifts the image by approximately 10° as long as patients do not neutralize the effect by making a compensatory eye movement of 10°. There is evidence that subjects with normal vision can adapt to the effects of the prism (44). Rosetti et al (45) have recently reported using active prism adaptation in patients with neglect rather than hemianopia. It remains to be seen whether this technique will provide an aid to visual rehabilitation in patients with neglect let alone in those with HVFDs.
Despite total destruction of the striate cortex, or even hemispherectomy, 20% of patients with HVFDs remain able to discriminate, without consciously perceiving, attributes of visual targets that are presented tachistoscopically to their blind hemifields in a forced choice context (46,47). There are several theories concerning the mechanism of this “blindsight” (48,49). One theory is that “spared islands” of striate cortical neurons that have survived injury retain their regular projections to extrastriate cortical regions and mediate residual visual function (50). But when no functional striate cortex remains, as after hemispherectomy, this explanation cannot be valid. In that case, blindsight may be mediated by extrageniculostriate pathways projecting to subcortical structures, including the superior colliculus and the pulvinar, and ultimately to the ipsilesional extrastriate cortex via tecto-tectal pathways (48,51,52). An alternative explanation invokes cortical plasticity.
Hemianopes have been taught to detect targets in their defective hemifields using blindsight retraining techniques in which they practice discriminating visual stimuli presented as part of forced-choice paradigms (17,53-56). The consensus had been that this training merely induced patients to make larger saccades into their blind fields, rather than using blindsight. However, recent fMRI (functional magnetic resonance imaging) studies have highlighted an affective component to blindsight in mediating the perception of unconscious emotional expression via the amygdala (57,58) demonstrated by the successful forced choice discrimination of positive versus negative facial expressions projected into the blind hemifield. Further functional studies with these patients have demonstrated successful fear-conditioning (59-61) whereby the presentation of a bland visual stimulus to the blind field is not consciously perceived but produces a fear response in the amygdala. This raises a further potential route for rehabilitation: could blindsight serve to condition useful, adaptive responses in patients?
Compensatory Oculomotor Strategies for Visual Exploration
Working with the concept that hemianopes naturally make strategic eye movement adaptations to overcome field loss, several groups have attempted to develop training programs aimed at systematically reinforcing these compensatory eye movements, thereby fortifying and enlarging the functional field of visual search. Normal daily activities apparently do not achieve the same effect.
There is limited evidence that patients can successfully adapt to their hemianopias with training in visual search (1,25,27,30,62). Training programs comprise three major steps: (1) practicing large saccades into the blind field in place of the inappropriately small saccades normally made by hemianopes; (2) practicing visual search on projected slides to improve the spatial organization of eye movements; and (3) applying both techniques to real-life scenarios. Various parameters have been used to judge the success of these techniques, including improvements in response time and error rates during visual search, enlargements in the visual field and visual search field (defined as the perimetrically measured area that a patient can actively scan using eye movements without head movements when searching for a suprathreshold stimulus), and improved proficiency in activities of daily living assessed objectively and with questionnaires.
After training 30 patients with HVFDs in daily sessions, Zihl (62) initially reported that the visual search field expanded from 10° to 30° within four to eight sessions. Kerkhoff et al (30) validated these results with 92 hemianopic patients and an additional 30 patients with hemineglect, whose search field increased from 15° to 35°. In a further study, Kerkhoff et al (27) quantified the functional benefit of this training program. After 25 treatment sessions, 22 patients showed a 50% reduction in the time taken to find objects on a table, complementing the subjective improvement elicited in a questionnaire that rated disability. Error rates and response times in visual search had significantly improved. Significant visual field and visual search field expansion were also confirmed. After treatment, 91% of this group returned to part-time work. Zihl (25) proceeded to record the eye movements of eight hemianopes before and after training in visual search, and highlighted how the improvements in the organization of their scanpaths contributed to the shortening of their response times (25).
More recently, Nelles et al (29) have trained 21 patients in visual search and found that training improved detection and reaction to visual stimuli without expansion of the visual field. Patients reported significant functional improvements in a daily living questionnaire.
Visual Field Recovery
Enormous controversy has surrounded the question of whether any training techniques can significantly reverse visual field loss in hemianopes (1). In a series of experiments in patients with HVFDs, Zihl (63-65) used a technique that involved repeatedly determining light thresholds at the visual field border (64-66). In most cases, the visual field enlargement did not exceed 5° but there were individual cases with remarkable recovery. Kerkhoff et al (27,30) and Pommerenke and Markowitsch (67) observed minor expansions of the field border by 1° to 6.7° in analogous experiments. Balliet et al (68), however, were unable to reproduce Zihl's results (see Zihl's response) (69).
Sabel et al (72) have reopened the debate by publishing a series of experiments based on sounder methodologies developed in response to the deficiencies highlighted in previous publications (70-73). Using a domiciliary PC-based stimulus system, they randomized patients with HVFDs to receive an active visual restitution training (VRT) stimulation program or a placebo stimulus program for 1 hour daily, 6 days per week, for 6 months. In the active VRT program, patients were required to respond with a key press to hundreds of repetitive visual stimuli presented in the transition zone between the intact and damaged visual field sector. Responses were monitored by the computer and the stimulus pattern was modulated in accordance with the responses. Stimuli for the placebo program were presented only at fixation. In the study, 95% of the actively treated patients demonstrated a central visual field gain of approximately 5° into the hemianopic field, an enlargement that restores the parafoveal field that is functionally significant for reading. None of the control subjects improved. Of the patients receiving the active VRT program, 72% reported subjective improvement in vision, compared with 17% of the control group. The authors demonstrated that VRT using a white dot stimulus generalized to color and pattern recognition (70), although additional treatment with specific color or shape recognition training resulted in a more pronounced improvement of those functions (69). This technique has now been commercialized (NovaVision AG) and received approval from the United States Food and Drug Administration in 2003.
To explain the mechanism underlying visual field expansion, Sabel et al (71,74) have hypothesized that regular visual stimulation at the damaged visual field border region by VRT could reactivate surviving neurons, providing small islands of residual vision in the cortical region that subserves that field. Considering that survival of a mere 10% to 15% of neurons in a damaged region has been postulated to be sufficient for recovery of basic visual functions (75), repetitive stimulation may lead to reactivation of these neurons, possibly with expanded receptive fields and improved synaptic connectivity (74).
However, a recently published study by Sabel's group and scientists in Tübingen, Germany (76), in which the visual field was tested independently using a scanning laser ophthalmoscope that controls for visual fixation, failed to find any significant improvement in the visual field defects, although many of the patients noted a subjective impression that they had benefited from the VRT. In an accompanying editorial, Horton (77) suggests that during VRT visual fixation is inadequately controlled, so the reported mean 5° field recovery could be explained by the frequent saccades hemianopic patients make toward their scotoma to maintain surveillance of blind areas in their visual fields (24,26). The visual field improvement therefore may be a function of the method of visual field assessment and fixation control. In an earlier study in which the visual fields were tested before and after VRT using a Tübingen automatic perimeter, no field improvement was noted, although this was not the case when the visual fields were assessed using the same software program as had been used for the VRT (73).
Patients with hemianopias have reading difficulties that reflect the laterality of the visual field defect. Left hemianopias cause difficulties with the return eye movements required to find the beginning of a new line. Right hemianopias cause more severe reading difficulties, with loss of the anticipatory parafoveal scanning process and a characteristic reading disorder termed “hemianopic dyslexia” (78,79). This disordered reading is reflected in the disruption of reading eye movement scanpaths, which show prolonged fixations, inappropriately small amplitude saccades to the right, and many saccadic regressions. Patients develop individual tricks to overcome these problems, using rulers to keep to the correct line of text or turning a page of text by 90° so that left-to-right reading becomes above-to-below reading (80).
Several groups have postulated that by retraining and improving the disordered eye movements, reading performance will improve. Computer-based systems should have many advantages in delivering and monitoring VRT programs. A computer-based VRT system designed by Zihl (1,81) was used to train a group of 96 patients with HVFDs. At the end of training, patients were able to read faster and with fewer errors, and eye movement recordings demonstrated fewer fixations, shorter fixation periods, and larger saccadic jumps. Patients with right HVFDs were more disabled and required more training sessions than did patients with left HVFDs (33 sessions compared with 26), and at the end of training they had not improved as much as those with left HVFDs (1). Kerkhoff et al (82) used an identical protocol to train a group of 56 hemianopic patients for a period of approximately 3 weeks (mean = 13 sessions). This group also demonstrated improved reading, and for both patient groups the improvement was maintained at a follow-up of 6 months to 2 years (1).
Although the benefits of rehabilitation in patients with HVFDs are often perceived as offering marginal gain, it is likely that this perception may underestimate their real value because the confidence and boost in self-esteem that they give patients is not recognized. The rehabilitation programs currently available or undergoing trial are complex and labor-intensive, and in general they require relatively specific facilities for their implementation. Therefore, the emphasis is shifting to the development of simple, user-friendly techniques that patients can practice in their own homes, causing minimal disruption to their daily lives.
Whether saccadic visual search training provides a successful treatment of patients with HVFDs remains unanswered, largely because many of the various studies have not been adequately controlled, and have not convincingly demonstrated improvements in visual search performance in activities of daily living. In these studies, patients have acted as their own controls (within-subject repeated measure design) and there are no control groups or placebo treatments. Given that patients can improve their performance in visual search with training, it is now necessary to address the specificity of the technique against a placebo condition. A randomized controlled trial with patients who are not trained is needed to assess therapeutic efficacy. However, because of the heterogeneity of underlying lesions, it would be difficult to ensure that control and experimental groups are comparable. A study with a cross-over design may be preferable technically but unacceptably long for patients.
In response to clinical need, visual search training techniques are now available. For example, we have developed a domiciliary rehabilitation tool for patients with HVFDs based on a visual search paradigm that is inexpensive and easy to use (63). We have trained 29 hemianopic subjects in their own homes on a dedicated television monitor using a portable computer. Our data show that most patients not only become significantly faster at performing visual search in the laboratory setting but also perform significantly better in validated activities of daily living. Patients rate themselves as less disabled in a visual disorder questionnaire (63). However, there was no evidence for any visual field recovery. The program is now available to patients on video but still needs validation in a placebo-controlled trial.
With respect to computer-based VRT, the domiciliary PC-based design of the system certainly increases the program's convenience and cost efficiency. Although the magnitude of visual field expansion appears small (5°), such gains in the central field would unquestionably be useful to patients exploring their immediate environment. However, the most recent study (76) casts doubt on its effectiveness.
There have been great advances in the field of optical aids with Peli's pioneering multiplexing technique. However, all optical aids require expert fitting in specialist centers and are available only to a minority. Although definitive evidence of their clinical effectiveness is still lacking, computer-based or video-based visual training programs are potentially more readily available and free of side-effects.
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