Acquired visual field defects rehabilitation: Critical review and perspectives




Abstract


Visual field deficit (VFD) is one of the most commonly observed symptoms following brain injury. Persistent VFD and defective exploratory oculomotor scanning patterns often cause severe impairment in daily activities, particularly as regards visual exploration and reading. Homonymous hemianopia is consequently a powerful negative predictor of patient outcome. In spite of these quantitative and qualitative factors, there currently exists no consensus on rehabilitative therapy and treatment. Different approaches have nevertheless been developed, all of them having one therapeutic principle in common; repeated practice of a specific visual task, with the hope/expectation that improved performance will extend to a wide range of ecologically useful visual functions. The four main available methods aim at replacing part of the intact visual field with part of the damaged visual field (optical therapy using prisms), at partially restoring the lost visual field region (restorative therapies), at stimulating detection capacities in the blind field (stimulation or blindsight) or at substituting for the lost region by reorganizing the control of visual information processing and eye movements (compensatory therapies). This review explores the key data relative to these different approaches in terms of behavioral or imagery results. It also aims at critically analyzing the advantages and limits of each one. The importance of strict assessment in terms of deficiencies or disabilities is underlined. Finally, upon consideration of these data taken as a whole, it is suggested that efficient treatment would probably have to associate general components and more specific elements, according to what may be done with regard to other aspects of cognitive rehabilitation.


Résumé


Les déficits homonymes du champ visuel font partie des symptômes les plus communs observés après lésion cérébrale. Ces anomalies sont particulièrement invalidantes d’un point de vue fonctionnel, induisant d’importantes difficultés pour l’exploration visuelle ou la lecture, avec des répercussions notables dans la vie quotidienne, constituant ainsi un facteur de mauvais pronostic fonctionnel. Malgré cette importance quantitative et qualitative, il n’existe à ce jour pas de traitement clairement établi ni prise en charge consensuelle. Néanmoins, un certain nombre d’approches différentes ont été développées pour essayer d’améliorer la gêne fonctionnelle des patients au-delà de l’évolution spontanée, pouvant être réparties en quatre groupes : (i) les aides optiques ; (ii) un entraînement à visée restaurative pour récupérer la fonction visuelle perdue ; (iii) la stimulation des capacités de détection au sein du champ visuel aveugle ( blindsight ) et enfin, (iv) l’entraînement à la recherche visuelle pour améliorer l’efficacité de l’exploration visuelle du côté déficitaire. Cette revue explore les principaux résultats de ces techniques (données comportementales et d’imagerie) et souligne l’importance d’une évaluation rigoureuse et systématique en termes de déficience comme de répercussions fonctionnelles. Elle s’attache aussi à analyser de façon critique les points forts et les limites de chacune de ces approches. Enfin, au vu de l’ensemble de ces éléments, il est proposé qu’un traitement efficace des déficits acquis du champ visuel doit probablement associer des composantes générales et des éléments plus spécifiques, en accord avec ce qui peut être conduit dans d’autres domaines de la réhabilitation cognitive.



English version


Visual field (VF) loss results from damage to the retrochiasmatic visual pathways and is among the most commonly observed symptoms following brain injury. Lateral homonymous hemianopia (LHH), the most frequent form of acquired VF impairment , denotes VF amputation in the area contralateral to the lesion that affects the two eyes and may be attributed to retrochiasmatic damage. Let us recall that the primary visual pathways correspond to the neuronal pathways coming from the retina via the ganglionary cells, and that most are projected through optic radiation at the level of the dorsal lateral geniculate body of the thalamus and then at the level of the striate or the primary visual cortex, which is located at the level of the occipital pole (V1 or Brodmann area 17). The ganglionary cells located in the nasal field of each retina emit axons that cross in the optic chiasma, with the axons of the cells located in the temporal retina remaining on the same side. As a result, each visual cortex receives an image originating in the two eyes and each visual half-field is projected into the opposite cerebral hemisphere. This reticulo-geniculate-striate route represents the main pathway for transmission of visual information between the eye and the cortex. V1 is consequently a critical site in perceptual processing of the basic visual characteristics of any stimulus (orientation, contrast, localization) , and is also the primary source of visual information for a multitude of other, superior extrastriate visual cortical areas. Damage to the central visual structures may be accompanied by a phenomenon of macular sparing corresponding to the preservation of foveal vision; the phenomenon is frequently observed following a cortical lesion but may also accompany other lesional sites on the visual pathways, and it may be due to recovery of the crossed and uncrossed projections of the ganglionary cells intervening in central vision. As a result, damage to V1 or its retrochiasmatic afferents is likely to produce major visual defects such as LHH in cases of unilateral damage and cortical blindness in cases of bilateral damage; this is due to the key role of V1 in transmission of visual information to the secondary and associative visual cortical areas. However, it has been demonstrated that subjects presenting with cortical blindness have not lost all their visual capacities in a portion of the field known as “blind” . Some patients indeed possess some degree of residual sensitivity to movement and/or shape and/or color . Unlike normal vision, this preserved sensitivity is most often unconsciously present, and that is why it is termed “blindsight” . Residual vision functions may nonetheless greatly vary from one individual to the next in terms of the affected visual field proportion, residual visual processing quality, and the degree of awareness associated with the process .



Lateral homonymous hemianopia: epidemiological data and functional impact


In a majority of cases (40 to 90%), LHH results from a vascular lesion in the area of the posterior cerebral artery or the middle cerebral artery , but it may also be observed in cases of traumatic, infectious or tumoral damage . The reported frequency of post-cerebral vascular accident (CVA) visual field deficit (VFD) ranges from 8.3 to 25% . Approximately 20 to 30% of the patients admitted to a neurological rehabilitation center present with a VFD and among them, 70% exhibit a spatially disorganized visual search strategy .


Moreover, the visual field deficits are more often than not associated with motor, sensory and/or cognitive deficits that combine to aggravate functional loss. And even when considered independently of these associated syndromes, VF anomalies are in and of themselves particularly invalidating from a functional standpoint, entailing impairment as regards reading , visual exploration, driving and movement in complex visual environments along with major repercussions in daily life, at home and on the job . More precisely, in terms of overall autonomy and taking into account a frequently associated motor deficit (hemiplegia or hemiparesis), the likelihood of acquiring relative autonomy or baseline functioning (Barthel index ≥ 60) decreases by more than 20% in the event of VFD; similarly, the likelihood of independence in walking (distance > 45 meters) in 14 weeks of clinical evolution decreases by 3 to 35% in the event of hemianopia . In other studies, it has been shown even when assessed on the basis of simple considerations such as the patient’s return home subsequent to a CVA , VFD constitutes a factor in poor functional prognosis .


Given these different elements along with the epidemiological data pertaining to CVA (130,000 new cases in France each year, the first cause of acquired disability in adults), it would appear particularly critical not only to carry out a precise evaluation, but also to be able to optimize rehabilitative care in such a way as to maximally limit the incapacities and activity restrictions occasioned by visual deficits, thereby going beyond the possibilities of spontaneous recovery.



Spontaneous evolution following lesion



Plasticity following lesion


While spontaneous recovery may indeed be observed following damage to the primary visual pathways, degree of recovery differs, as it depends largely on the underlying disease and lesion topography; more often than not and on an overall basis, it is relatively limited. Hier et al. emphasized recovery in about 30% of their LHH patients in a maximum time lapse of 8 months. A more recent review brought to light a possibility of spontaneous favorable evolution as high as 50%, with most recovery once again observed over the first 3 months, with only minimal progress reported after 6 months. In cases of ischemic LHH, Gray et al. recorded complete VF recovery in less than 10% of the cases studied. In cases of complete initial damage, such recovery is maximal over the first 10 days. When the defect is incomplete, improvement is maximal within 48 hours and minimal more than 10 to 12 weeks after injury . Finally, in addition to such recovery of visual functions, there may develop a deformed perception of the visual environment (distortion of objects at the edge of the blind quadranopsic VF in a patient ).



Spontaneous behavioral adaptation


Interestingly enough and complementarily to visual recovery in the narrow sense of the term, patients presenting acquired visual field defect also develop post-lesional modifications on oculomotor behavior. Some studies have shown that they could compensate for their visual loss by modifying their eye fixation strategies and directing their gaze to the blind hemifield . Even if the patients carry out a pattern of hypometric saccades on the blind side , that is to say quick eye movements that are not strong enough to reach the visual target, they are able at the same time to carry out extra saccades towards the “blind” visual field . More particularly, it was noted that when simple patterns were being observed, the fixation point was displaced towards the blind side, which meant that most visual activity was being conducted in the intact hemifield, thereby lending itself to interpretation as a compensatory strategy . Pambakian et al. have recorded the ocular movements (saccade and fixation parameters) of LHH patients gazing at images of real-life scenes. Their results show that in cases of injuries incurred over the previous six months, patients maintain eye fixation patterns close to those of normal subjects; after six months, on the other hand, the patterns are different, which means that a spontaneous strategy of compensatory eye movements may have evolved. Even though exploration generally begins on the healthy side , visual search on the injured side remains more time-consuming, regardless of any possible visual or spatial neglect . Having been observed with regard to different tasks , aiming the gaze at the blind VF may be considered as a compensatory strategy that naturally develops subsequent to a homonymous deficit in the visual field and allows for partial palliation of the loss of visual information on the injured side of the space . It should nonetheless be noted that in the event of visuo-spatial neglect, the concomitant presence of left-side LHH negatively affects exploration of ipsilateral space , with a possible difference in the neglect-LHH combination according to the visuo-spatial task .


Spontaneous VF recovery may thus be expected in only a limited number of patients, and the consequences of this spontaneous plasticity for perception would appear to be correspondingly limited in terms of amplitude, time lapse and impact on visual functioning in daily life. In a parallel manner, behavioral adaptations are essentially observed at the oculomotor level, with little if any repercussion on incapacities.


Given these limitations, it is important to know what may now be done for the great majority of patients in order to compensate for this visual deficit and its functional consequences.



The therapeutic approaches developed


Up until now, in spite of the impact and qualitative as well as quantitative importance of these disorders, there has not existed any clearly defined and established treatment or consensus on caretaking with regard to acquired VFD . However, for close to 20 years a number of different approaches based essentially on visual training techniques have been developed in order to try to lessen the patients’ functional disturbances and to bring about overall improvement.


A recent review precedes its treatment of therapeutic approaches with consideration of two major pragmatic and scientific aspects. Firstly, the acquired VFD does not have homogeneous repercussions on the different visual tasks encountered during daily activities. For example, a 2-to-3-degree improvement in parafoveal vision may be fundamental in heightening reading speed, but will have no impact on the qualitative or safety-related aspect of automobile driving. It is consequently important, not only when evaluating, but also – and especially – when organizing therapeutical intervention, to bear in mind both the nature of the visual function to be reeducated and the precise functional contextual elements being assessed. Secondly, and this postulate pertains to the scientific approach per se, quality in the evaluation treatment efficacy can be ensured only when the proposed therapeutic care procedures are comprehensively compared with a control therapy; this is especially crucial insofar as up until now, effort in terms of time and involvement has often exercised a determining role in the approaches having been developed. These parameters should be taken into account when reading the different results existing in the literature.


The principal rehabilitation strategies developed to date may be grouped according to four different types of caretaking procedures ( Table 1 ): (i) optical assistance, such as prismatic corrections aimed at VF relocation; (ii) restorative training aimed at recovering the lost visual function; (iii) stimulation of detection capacities in the blind VF (blindsight); (iv) visual search training aimed at enhanced efficacy of visual exploration of the defective side (see reviews in ).



Table 1

The different reeducation approaches developed in the framework of the reeducation of acquired visual field deficits and the main studies on the subject. For each study mentioned, the number of patients, the existence of a control group and/or therapy and the different parameters measured have been indicated.




























































































































































































































































































































































































































Rehabilitative approach Original studies Number of patients ( n ) Control group Parameters measured
Optical assistance / / /
/ / /
/ / /
39 (18 +21) Y (with or without) Visual perception tests, Barthel index
22 N Duration of prisms wearing, level of satisfaction
/ / /
9 N ADL questionnaire
12 N Duration of prisms wearing, VF, subjective evaluation of obstacle avoidance
10 Y (2 types of prisms) (cross-over) Visual aptitudes (mobility, recognition, daily living); follow-up duration, VF, attention, driving (simulator)
43 N Prism wearing maintained, mobility questionnaire
23 N Prism wearing maintained, VF, quality of life
Restorative approaches 12 N VF, VA, color perception, sensitivity to light/to contrats
14 N VF, VA color identification
55 (31 +24) Y (with or without) VF, sensitivity to light, recognition colors and shapes reading, subjective evaluation (reading, obstacle avoidance)
14 (11 +3) Y (with or without) VF, discrimination shapes and colors
38 (19 19) Y (placebo [fixation]) High-resolution perimetry (HRP), VF, subjective improvement
32 (19 +13) Y (placebo [fixation]) HRP, VF, shape and color detection
22 (16 6) Y (placebo [fixation]) Long-term follow-up (HRP, VF, shape and color detection)
1 N HRP, subjective evaluation ADL
69 N (retrospective VRT) HRP, subjective evaluation ADL
5 N VF static and kinetic, VEP, evaluation questionnaire
16 N HRP, VF, subjective questionnaire ADL
19 (10 + 9) Y (VRT ± attention index) HRP, VF
15 N HRP, VF, ocular movement recording during therapy
1 N VF static and kinetic, VEP, evaluation questionnaire, PETscan
23 N (attention index alone) HRP (stimulus detection rate and reaction time)
23 (9 + 7 +7) Y (VRT simple/costimulation) HRP, VF, ocular movement recording during therapy
302 N HRP, VF, ocular movements, subjective evaluation ADL
20 N VF static and kinetic, VA, vision shapes and colors, ADL
6 N HRP, fMRI
161 N (retrospective VRT) HRP (stimulus detection rate)
3 N VF static and kinetic, VA, visions shapes and colors, ADL
18 Y (standard VRT/extra-striate VRT) (cross-over) HRP, VF, NEI-VFQ questionnaire, reading, ZVT
11 N VF, ocular movement recording, reading
8 N VF, ocular movement recording, fMRI
Modelization Predictive efficiency factors for VRT (multivariate regression models)
Predictive VRT model
Criticisms 12 N CV static and kinetic
17 N CV (microperimetry), fixation monitoring, reading, subjective modifications
16 N CV (microperimetry), fixation monitoring, reading, subjective modifications
Blindsight stimulations / N Detection and localization of stimuli in the blind VF
/ N Detection and localization of stimuli in the blind VF
3 N VF static and kinetic, ocular movement recording (saccades)
12 N Spatial frequency detection, contrast detection, VF, subjective evaluation
2 N VF, fixation monitoring, magneto-encephalography
1 N VF, fixation monitoring, magneto-encephalography, fMRI
9 N VF, motor and verbal target localization, identification of letters
5 N VF, luminance detection, contrast sensitivity, movement sensitivity
Compensatory approaches
22 N VF, visual search field, object search time, subjective evaluation
14 N VF, visual search time (targets/distracters), oculomotor parameters a
21 N VF, target detection, RT, ADL scale
29 N Visual search (RT, errors), VF, visual search field; ADL (tasks + questionnaire)
ADL (tasks + questionnaire)
28 N Real driving test, visual attention, CVD questionnaire
Visuo-spatial tests, VF, VA
8 N VF, visual search, reading, questionnaire ADL
28 (15 + 13) Y (exploratory saccades/flicker) Visual search (RT, fixations), VF, reading, quality of life score (WHOQQL-BREF)
12 Y (visual/audiovisual) (cross-over) Oculomotor parameters a , reading, visual exploration time
8 N VF, fMRI, oculomotor parameters
42 (21 + 21) Y (exploration/attention + exploration) VF, visual search, reading, questionnaire ADL
Hemianopic alexia 56 N VF, reading
20 N VF, neglect test, reading, oculomotor parameters
32 N VF, reading
120 N VF, reading
19 Y (OKN/sham) (cross-over) VF static and kinetic, overall neuropsychological evaluation, reading (texts, words)
Ocular movement recording
40 (20 + 20) Y (verbal/non-verbal material) VA, VF kinetic, reading, visual exploration, subjective evaluation
Ocular movement recording

Y: yes; N: no; ADL: activities of daily living; VF: standard parimeter Visual Field; VA: visual acuity; VRT: visual restitution training; fMRI: functional magnetic resonance imaging; NEI-VFQ: National Eye Institute-Visual Function Questionnaire; WHOQOL-BREF: World Health Organization questionnaire on quality of life; ZVT: Zahlen Verbindungs Test; RT: reaction time; CVD: cerebral visual disorder; OKN: OptoKinetic Nystagmus.

a Saccades (latency, amplitude, direction) and fixations (localization, duration).




Optical assistance


Optical therapy consists in the use of optical assistance aimed at increasing visual scene perception. Such enhancement can be achieved by relocating and deviating the blind VF part towards the healthy VF part and by extending VF perception towards the blind VF. This objective may be reached through use of a small lateral mirror placed on glasses opposite the blind VF, which is then observed as in a rear-view mirror . Most often, the optical assistance consists in prismatic lenses. This was the first method to be developed in the framework of acquired VFD rehabilitation, and despite the lack of rigorously controlled clinical trials, it has yielded some interesting results.


The prisms may be included in a lens or a plastic membrane fixed on the lens, with the base of the prism being oriented towards the hemianopsic field. Light is thereby refracted in a new position. Several means of applying the prism may be used: sector or full binocular, sector monocular. Placement of the sector binocular prisms entails application of the prisms on the hemianopsic portion of the two lenses with the objective of deviating the healthy VF towards the blind VF (there is no expansion of the VF). To avoid interference with macular vision, the prisms are shifted 1 to 2 mm from the pupil center. One of the drawbacks is that only when the gaze is directed towards the prisms are they useful. This method is nonetheless the one that has been the most widely utilized . In particular, Rossi et al. employed this type of system in 39 patients presenting with LHH or unilateral spatial neglect (15-diopter peripheral binocular prisms). Their results show improvement in visual tasks without functional repercussions following use of the prisms. As for use of full binocular prisms, it necessitates the placing of prisms on the two lenses, the VF being tilted or deviated towards the base of the prisms. There have been no relevant clinical studies pertaining to this type of procedure.


Use of sector or peripheral monocular prisms appears to be more promising. A prism is placed on the lens homolateral with regard to the hemianopia, that is to say widthwise across the upper and the lower portions of the lens, thereby inducing optical deviation, whatever the lateral position of the gaze. In addition to the deviation, the technique may allow for expansion of the visual field following a necessary phase of training and adaptation and provided that the lenses are worn throughout daily activities. Having applied this technique, Peli has highlighted VF expansion as high as 20% in cases ( n = 12 patients) where 40-diopter prisms are worn, but without a control group for the sake of comparison or standardized measurements with regard to satisfaction (see review in ). A more recent, multicenter study employed the same procedure in 43 patients and demonstrated satisfactory tolerance of the apparatus over a substantial time span (follow-up as long as 1 year) along with concomitant functional benefits such as obstacle avoidance during movements. Finally, Giorgi et al. studied the degree of tolerance and functional utility of this type of procedure in 23 patients. Two thirds of them continued to wear the prism until the end of the study (mean: 9 weeks), while the long-term proportion (> 8 months) decreased to 42%. The main functional benefits were noted in the framework of movement, with some difficulties in crowds, when descending stairs, and while reading.


Whatever the success rates of these different forms of optical assistance, training and adaptation remain constraining and costly in terms of both time and energy. And while they may at times be proposed, their efficacy has yet to be clearly demonstrated in a controlled setting.



The restorative approach


The restorative approach revolves around the idea of the plasticity of the visual system and its ability to adapt to post-injury modifications. As early as 1978, Poppel et al. had shown in a patient having presented with posterior CVA that the training of visual functions (repeated testing with a perimeter) could modify the VF. Zihl and von Cramon and Zihl observed similar “training” effects through use of a technique requiring repeated determination of a lighted detection threshold in the border separating blind VF from healthy VF. In most cases, even though some instances of remarkable recovery have been reported, VF expansion failed to exceed 5%. Kerkhoff et al. and Pommerenke and Markowitsch observed less pronounced expansion (from 1° to 6.7°) in analogous experiments. Balliet et al. were unable to reproduce similar results. It became important to know whether or not this kind of training technique could be repeated so as to actually yield recovery of the lost VF.


Kasten et al. revived debate by developing practices aimed at stimulating the VF border zone between the defective area and the intact area along the vertical meridian with the objective of improving the functioning of these partially preserved visual areas (“striate system restoration”). The benchmark study had facilitated development of software set up in a personal computer delivering binocular visual stimulations on a screen in a transition area located between the intact VH and the defective VF. The patients received either active training (Visual Field Restitution Therapy VRT) or placebo-based training in accordance with a stimulation program taking place one hour a day (two 30-minute sessions) and 6 days a week over 6 months. In the active program, patients had to answer by simply pushing a button in response to the hundreds of repeated visual stimuli presented in the predetermined transition zone. Their responses were controlled by the computer and thereby modulated the stimulus pattern. In the placebo program, the stimuli were presented only at the fixation point. The results show that 95% of the patients in the group under treatment registered hemianopsic VF expansion of approximately 5%, with no significant gain for the control group; the expansion was observed by means of a form of high-resolution perimetry (HRP) developed by the authors but not observed in conventional perimetry. Moreover, subjective vision improvement was reported for 72% of the same patients under treatment (as opposed to 17% in the control group). The explanatory hypothesis put forward by the authors is that regular and repeated stimulation of the zone bordering the defective VF could reactivate surviving neuronal activity, and that survival of 10 to 15% of the injured neurons might suffice to restore basic visual functions , thereby leading to small islets of residual vision in the corresponding cortical area through expansion of the reception fields and improvement in synaptic connectivity .


However, the reported efficacy remains controversial on account of possible non-controlled confounding factors such as light dispersion or deviation of the fixations that could have an impact on measurements of visual field “recovery” . Three main lines of argument contribute to the polemic.


The first source of controversy pertains to the perimeter techniques employed. Three different types of perimetry (or campimetry) have indeed seen use: HRP (already mentioned), conventional perimetry (TAP) and scanning laser ophthalmoscope (SLO). Advocates of VRT have focused upon their own method (HRP), which is the main usual tool in both assessment and therapeutic care but does not permit satisfactory monitoring of fixation. As a result, ambiguities and divergences have appeared in a number of studies, particularly as regards the transition zone evaluated in terms of HRP and relative scotoma measured in TAP. In another study, Reinhardt et al. independently tested the VF by using a device allowing for monitoring of visual fixation while training was taking place; even though a number of patients mentioned subjective visual improvement, there was no demonstration of any significant objective VF improvement. Horton and then Grant then went on to suggest that mean VF recovery following VRT (about 5°) could be explained, given the lack of fixation monitoring, by the saccades frequently effectuated by patients in the direction of the defective VF (a spontaneous compensatory pattern previously noted . Some measurement artifacts may also be due to attentional changes . One way of testing the technique’s credibility would consequently necessitate demonstration of a decrease in relative scotoma (corresponding to VF expansion in the transition zone) by conventional perimetry combined with assiduous monitoring of central fixation quality during assessment as well as training. In response, Kasten et al. more specifically studied the ocular movements in 15 patients both before and after 3 months of VRT; on a parallel track, the VF was measured by conventional perimetry and high resolution, and fixation time was measured with an Eye Tracker system. The results show no modification of ocular movement parameters in terms of either direction or amplitude. However, they do not directly answer the question as to how fixation is monitored during treatment, in which high-resolution perimetry is used. The role of attention has also been underlined by these authors in a double stimulation paradigm suggesting association of an overall effect with a specific form of training. It also bears mentioning that a large-scale European multicenter study has been conducted by Mueller et al. , who used different types of perimeters (HRP and conventional) to measure the VF before and after VRT. The gain that appears in terms of target detection is not correlated to oculomotor parameters and is accompanied by subjective improvement (semi-structured questionnaire) in spite of the lack of a control group.


Finally and interestingly, Bergsma et al. have studied the development of possible improvement following VRT through application of the Goldman kinetic perimeter test before, after and especially during the training (all 10 sessions), with the fixation being closely monitored. Their results show a gradual shift of the border zone healthy VF/defective VF that is associated with a deviation of visual attention, without development of supplementary compensatory oculomotor movements.


A second line of criticism pertains to injuries or lesions . Precise identification of lesion histogenesis and accurate topography of post-geniculate lesions are often missing in studies devoted to VRT, even though these elements may be crucial as regards both clinical description (presence or absence of macular sparing) and potential therapeutic effect (tumoral or vascular process).


Finally, the third line of criticism is related to explanatory mechanisms. The different hypotheses aimed at explaining the beneficial effects of VRT are largely predicated on the notion of cortical plasticity, and based on data taken from the animal-centered literature. Moreover, the proposition according to which the repetitive activation produced by VRT may stimulate the plasticity process remains altogether speculative. That said, recent studies in functional imagery have opened up some avenues for thought. An initial study of a single case analyzing the clinical (perimetry and subjective questionnaire), electrophysiological (PEV) and imaging (PET scan) parameters showed a positive correlation between the different measurements before and after 3 months of training (subjective and VF improvement, appearance of a P100 component and increased cerebral blood flow at the level of the contralesional lingual gyrus). Marshall et al. used functional MRI to study brain activity before and 1 month after VRT ( n = 6 patients with right LHH). Their results show a modification of brain activity correlated with improved detection time in the border zone, particularly at the level of the right and left anterior cingulated cortex (ACC), the right dorsolateral prefrontal cortex and bilaterally at the level of the basal ganglia. A positive correlation likewise appeared at the level of secondary and associated visual areas (right occipitotemporal, mean temporal and inferior parietal lobule). These modifications are ascribed by the authors to the training process per se, without any parallel observation of VF expansion, which probably takes place at a later stage of the caretaking procedure. What remains to be determined is on the one hand the degree of activation ascribable to visual attention factors and the effects of training, and on the other hand the degree that may possibly be imputed to expansion of the VF border zone. Raemaekers et al. correlated conventional perimetry and retinotopic mapping (functional MRI) before and following 10 weeks of VRT ( n = 8 patients). The behavioral results showed significant VF expansion (1° to 7°) without any real modification in activity of the visual cortical areas, even if a tendency towards greater eccentricity was observed for a number of receptor fields. And there was no apparent evidence of representation extension of the VF impaired at the level of the primary visual cortex.


These objective data, which were gathered in a monitored setting taking into account some of the previously expressed reservations, should serve to modulate predominant skepticism. And yet, given the high variability of the results reported and the wide range of patients recruited, it would appear primordial, as is the case in the other areas of neurological rehabilitation, to be able to identify the patients who are likely to be the most responsive. It is probable that the expanded VF induced by VRT may be observable only in the cases of patients presenting with incomplete or partially reversible postchiasmatic lesions, a progressive gradient with regard to the loss of light sensitivity and/or residual metabolic and/or functional activations in the affected striate cortex . A predictive and more mathematical vision restoration model has recently been constructed and may one day provide guidance in the choice of most appropriate form of individual care.


Given all these different factors, as of now HRP perimetry systems are only confidentially used, and therapeutic caretaking by VRT remains controversial (even if recent findings tend to modulate opposition). Financial considerations probably tend to aggravate the existing scientific polemics .



Stimulation of detection capacities within the blind visual field (blindsight)


Initially developed on the basis of the data reported by Zihl , use of extrastriate visual pathways with the objective of repairing the visual functions secondary to striate pathway injury has recently taken on a new life, probably in the wake of VRT . As already mentioned, the convergence of a number of items (behavioral, psychophysical, electro-encephalographic, functional imagery) has come to establish the presence of a residual visual treatment process (despite the damage to geniculate-striate visual pathways) for which the patient’s conscious perception is either altered or absent (the blindsight phenomenon). Raninen et al. , for instance, trained two patients to perform a task in detection of a flickering light stimulus and also a task in identification of a flickering letter. The stimuli were located in the blind VF, at 10° or 30° eccentricity. After one year of intensive training, performances of the two tasks (detection and identification) were comparable to those recorded in an intact VF. Sahraie et al. trained 12 patients at an interval detection task, with the stimulus being characterized by spatial and temporal frequencies known to remain in the blind VF . After 3 months of daily training, the results showed improved detection rates with regard to low-contrast stimuli in trained locations, with heightened sensitivity in perimeter testing but without systematic correlation to conscious perception or awareness of these stimuli. In addition to these behavioral analyses, cortical modifications induced by this method have been shown to exist in a patient with ipsilateral representation of the VF who had been trained in several cortical areas including the primary visual cortex, thereby suggesting post-treatment functional reorganization possibly using a subcortical pathway solicited in the training. Applying the same principle of soliciting a residual visual treatment pathway, Chokron et al. subjected eight patients to forced-choice visual tasks for a period of 22 weeks. Evaluation before and after treatment showed (detection, identification and perimetry) showed improved behavioral performance correlated with an expanded VF, thereby suggesting possible improvement in explicit visual detection capacities through the use of unconscious capacities. More recently, Huxlin et al. trained five patients in discrimination of the overall direction of a light stimulus moving randomly in their blind VF. Their results showed that following training, the capacity to discern this overall direction is gradually recovered, but only within the areas included in the training. It nonetheless bears mentioning that the improvement carried over into contrast sensitivity and motion coherence (untrained parameters).


Through use of residual vision and provided that ocular movements be precisely monitored, intensive training of the blind VF can consequently improve detection performance and/or contrast sensitivity in the trained task, thereby suggesting the existence of perceptual learning capacities in the blind VF. A question nonetheless remaining open pertains to the specificity of the effects of the training with regard to retino-optic specificity, to the stimulus and/or the task; most often, after all, the improvements are limited to the trained characteristics. Given the complexity of the visual environment, the specificity of training effects is indeed crucial, not only from a theoretical standpoint, but also in the framework of efficacious rehabilitation strategy development. The other sensitive aspect of this type of caretaking consists in the necessarily intensive and repetitive training required before any improvement is achieved.



The compensatory approach


The use of ocular movements and the development of compensatory oculomotor strategies would appear to be a worthwhile way of compensating for the VF loss, since ocular movements constitute a patient-specific “tool” substituting for the lost visual area and perhaps likely to be employed spontaneously, provided that awareness of the VF defect exists. Moreover, the close and reciprocal connections between ocular motricity, attention and visual perception constitute a theoretical framework favorable to this type of approach . In addition, the phenomenon occurs spontaneously during the processes of recovery and/or compensation observed in post-ictus. Given these facts, several teams have endeavored to develop training programs aimed at systematically reinforcing these compensatory ocular movements and/or at correcting “errors” in adaptation, with the objective of invigorating and reinforcing the functional visual search field .


Training programs generally include three major stages: (i) carrying out large saccades in the blind VF instead of and rather than the small and inappropriate saccades usually performed by hemianopsic patients; (ii) carrying out visual searches on the scenes projected so as to enhance the spatial organization of ocular movements; (iii) applying these two techniques to real-life scenarios. The patients thereby intentionally learn how to displace their eyes and their gaze, and consequently the healthy VF/blind VF border, towards the area corresponding to their blind VF. This shift enables transmission of information from the blind VF to the healthy CF so that it may be perceived and processed efficiently. VF expansion has occasionally been achieved , the observed improvement being essentially ascribable to efficient oculomotor adaptation, which indicates a functional reorganization of the control of visual information processing and ocular movements during visual exploration and/or reading.


The training sessions are at least daily, and vary in duration from 30 to 40 minutes, with total caretaking duration ranging from 1 to 6 months. More often than not, the results show some improvement in visual search patterns with only marginal gains in terms of functional benefit, and the training requires a relatively specific set-up. Some studies have been conducted with a control group. Roth et al. compared in 28 patients the effects of training in performance of exploratory saccades as opposed to training in the detection of flashing stimuli. The results are encouragingly favorable to the active exploratory paradigm, since they show a significant decrease in the time devoted to visual research and scene exploration in the blind VF that is accompanied by an increase in the number of fixations and subjective improvement, without modification of the VF per se. The exploratory training being based on paradigms of visual search that evidently require visual attention, questions pertaining to the contributory role of the latter have recently been put forward. Lane et al. , for instance, had two groups of 21 patients undergo either exploratory treatment or attentional treatment followed by exploratory treatment. The results show that the two types of treatment both improve performances in the assigned visual tasks, but also that the transfer of efficacy may not be generalized to include all the tasks necessitating visual exploration; there was no significant effect, for example, on reading. These results strongly underline the key role of attention in rehabilitation from acquired visual field defects. Pragmatically speaking, the material needed in attention training is simpler and more accessible than other material. That said, more specific measurements of the different capacities for attention in the framework of controlled trials would appear necessary in order to confirm this interesting tendency (even if it is somewhat disappointing with respect to the results of the compensatory approach…). Nelles et al. conducted a functional MRI study in order to examine the effect of training in visual search movements on cortical control of the saccades. Eight patients with an occipital vascular lesion were initially included, with the first evaluation 8 weeks post-CVA, the second after 4 weeks of training, and the third and last 4 weeks after discontinuation. Their results show that training in the performance of ocular movements induces a modification of brain activation at the level of the striate or extra-striate cortex, and also at the level of the oculomotor areas. The fronto-parietal network controlling ocular movements would thus appear to be preserved. Moreover, the increased activity on the contralesional peristriate cortex is consistent with the data observed in cases of hemispherectomy and with the observation by Henriksson et al. pertaining to cortical reorganization.



Specific case of hemianopic alexia


Hemianopic alexia designates a singular, frequent and invalidating incapacity corresponding to an acquired reading disorder in patients presenting with an acquired visual field defect, in spite of strictly normal phasic functioning. Functional complaints quite often spontaneously originate with the patients themselves. Identification of the words and/or capacities to plan out or to guide the ocular movements needed in reading may be perturbed to varying degrees.


Several parameters, which it is important to evaluate, may be likely to interact with the intensity of the difficulties and with the functional impairment. The first crucial element is the notion of foveal or parafoveal damage or sparing . More specifically, patients with VF deficits affecting the parafoveal (±5° left or right of the fixation) or foveal (±0.5 to 1°) region present with major hindrances as regards the identification of words, as well as the planning out and guiding of the ocular movements needed in reading. This is translated not only by slowed reading, but also by the disorganized patterning of ocular movements, which itself translates an inadequately efficient oculomotor strategy. Letters, syllables and short words are often omitted, or else incompletely perceived words are incorrectly completed. These patients generally do not encounter difficulties when confronted with tasks of reading letter by letter or of spelling. The second important element to take into account is the laterality of the defect . In most cases, patients with a right lateral homonymous deficit are more severely affected than patients with amputation of the left VF – at least as regards left-to-right systems of writing and reading. In patients with a visual deficit of the left hemifield, functional repercussions are most often of a spatial nature (spatial alexia); they essentially have trouble backtracking along a line to recover the beginning, and their difficulties are at times associated with omissions of the beginnings of words and/or sentences. In these cases, analysis of the ocular movements does not show large-scale disorganization. Conversely, patients with right homonymous defects often show highly pathological oculomotor patterns, with a rise in the number and duration of the fixations and the reading saccades termed regressive (saccades towards the left to improve perception of a word located at the right), an increased propensity to re-fixate words, and more numerous and smaller saccades in the direction of the blind VF . These different elements are directly connected with the fact that the right homonymous defect deprives patients of important visual information as regards the form and location of the words following one another on a line, words that a “normal” reader employs so as to guide his performance of an efficient series of reading saccades. The processing of words consequently requires more time, and this has major repercussions on the speed and quality of lexical identification, thereby impeding comprehension .


As already mentioned in the framework of visual search, the development of spontaneous compensatory strategies has been observed and accompanied with improved reading performances . This is especially the case in patients presenting with a lesion limited to the primary visual cortex and preserving attentional control over visual processing and ocular movements. Most of the patients presenting with larger lesions, which affect the geniculo-striate pathways, find themselves unable to adapt to their reading difficulty . As regards reeducation-based approaches, most studies have focused upon visual exploration, with reading being occasionally considered as a secondary evaluation parameter. A recent review more specifically dwelt upon the question of rehabilitation of hemianopsic alexia. Only six studies have been primarily devoted to therapeutic care of this peculiar defect . On the basis of these elements, the author wishes to suggest the possible superiority of compensatory methods, which are designed to reorganize the control of ocular movements. One approach involving the repeated and systematic practice of the ocular movements specific to reading appears to be particularly promising . It consists in using a text to be scrolled from right to left, thereby creating an optokinetic nystagmus. The results show significant gains (compared with a control group) in terms of reading speed after 4 weeks of daily training, with a higher amplitude of saccades towards the right (specific directional effect). While the underlying mechanisms remain unclear, the positive medium-term effects (6 to 8 weeks) are encouraging.



Conclusion, future directions and perspectives


The studies carried out over recent decades tend to suggest that patients whose acquired VF deficits pronouncedly affect their daily activities may avail themselves of a certain number and a certain range of interventions, even though none of the latter predominates in terms of functional benefit. The methods appearing most efficient are based upon learning how to carry out large ocular movements towards the blind visual field, and they are aimed at transferring a maximum amount of information on the visual scene to the healthy VF. For the most part, these methods are predicated on active, voluntary, top-down saccade improvement techniques and on repeated drill-type exercises. They allow patients to activate an intentional strategy when they find themselves in a sensitive situation (such as a clinical context). But in most cases, they do not allow the patients to compensate for their defect in the most automatic situations encountered in daily life. Moreover, they necessitate a form of assiduity along with material and financial constraints that would hardly appear compatible with large-scale, routine implementation.



Development of bottom-up approaches


Given the limitations of the previously mentioned techniques, bottom-up methods, which short-circuit the need for awareness of the defect and the activation of voluntary processes, would seem to constitute an interesting alternative track. Their principle consists in acting upon the systems producing ocular movements, especially saccades, by means of their projections emanating from sensory-motor systems, in a more automatic, ascendant, or “bottom-up” fashion. Bolognini et al. have developed a new, compensatory approach revolving around a mechanism involving audiovisual integration processes, with certain neurons assuming a significant role in spatial orientation and with saccade movements responding to multimodal sensory stimuli . The patients were trained to detect the presented visual targets either separately, or together with an auditory stimulus. Therapeutic caretaking (a 4-hour daily session over a 2-week period) yielded interesting results in terms of visual detection and visual search in cases of combined stimulation. These results were recently complemented by the recording of eye movements in the framework of a similar paradigm ; in addition to confirming behavioral improvement, the recordings showed, subsequent to training, improvement with regard to oculomotor parameters (less fixation and refection, speedier and larger saccades). The improvement pattern was maintained over a year of follow-up.


Notwithstanding these promising factors, such caretaking remains particularly time-consuming and in fact also demands a considerable amount of conscious, voluntary and active participation. In a similarly interesting manner, preliminary findings ( n = 7 patients) suggest that training patients with an acquired VF defect by means of predictive saccades carried out through “jumping” movements in pursuit of a moving target that disappears and then reappears in a portion of the damaged VF might improve visual exploration immediately after performance of the training task (assessment with ecological tasks). Ongoing complementary studies are assessing the reproducibility of the results of this approach, which is simple and easy to implement, with regard to a larger subject population and in comparison to a control group. The questions of the pertinence of repeated sessions and of possible prolonged and/or cumulative therapeutic effects will also be considered, with a potentially encouraging cost-benefit ratio (time saved) that has yet to truly predominate in the field…



Perspectives


Aside from the pragmatic perspectives that the most recently developed approaches appear to open up, new works will indispensably complement the previously documented methods. In the framework of VRT, the exploration of mechanisms that might one day undergird VF expansion appears primordial. Application of this type of approach at an earlier stage might likewise be relevant, given the probability of higher sensitivity in terms of post-lesional plasticity. As for blindsight approaches, which are based on consistent neurophysiological data, results have been encouraging. Moreover, activation and stimulation of a non-conscious perception converges rather interestingly with more recently documented methods. And complementary investigations pertaining to compensatory strategies also need to be conducted. These methods, which appear at present to be the most promising (in terms of results as well as feasibility) still require supplementary specifications by means of controlled studies (type of stimulation and training, optimal protocol, modalities of application). Finally, some combination of these different methods could provide an additional track, for the purpose not just of possible addition of effects, but also with regard to potentialization or optimization.


Taken together or as a whole, these elements suggest that efficient treatment of acquired visual field defects shall probably have to associate general components with more specific factors, in conjunction with what has already been achieved in other areas of cognitive rehabilitation . Caretaking procedures might consequently include general visual attention training along with the learning of new skills and/or specific visual strategies with regard to pertinent functional activities (such as reading, for instance). Evaluation of visual deficiency, and more especially of its functional repercussions in terms of limits to activity and restrictions on participation would appear to be primordial prior to any therapeutic proposal, the objective being to optimally target individual difficulties and then, ideally, to put forward an optimally targeted, case-by-case approach.


Disclosure of interest


The authors declare that they have no conflicts of interest concerning this article.

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Apr 23, 2017 | Posted by in PHYSICAL MEDICINE & REHABILITATION | Comments Off on Acquired visual field defects rehabilitation: Critical review and perspectives

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