Neurovisual Rehabilitation in Cerebral Blindness

0 downloads 0 Views 2MB Size Report
field recovery, (2) to assess the transfer of treatment gains to functional outcome ... left-sided homonymous hemianopia and 15 had right-sided hemianopia.
ORIGINAL CONTRIBUTION

Neurovisual Rehabilitation in Cerebral Blindness Georg Kerkhoff,

PhD; Udo Münßinger, MA; Elke K. Meier, MA

Ob jective: The efficacy of a systematic trainingof saccadic eye movements was evaluated in hemianopic patients with three main objectives: (1) to determine the role of visual field recovery, (2) to assess the transfer of treatment gains to functional outcome measures, and (3) to evaluate the patients' subjective experience throughout therapy.

visual search field within the scotoma, visual search on projected slides with wide eccentricity, search times for identifying objects visually on a table (table test), and standardized rating of the degree of subjective visual impairment due to the field defect. All outcome measures were planned before initiation of the study.

Design: Within-subject repeated measures design. The mean follow-up interval was 3 months (ränge, l to 10 months).

Results: (1) Increase in visual search field size (mean, 30°). (2) Training-related visual field increases in 12 (54%) of 22 patients (mean increase, 6.7°; ränge, 2° to 24°). (3) Transfer of treatment gains to functional measures (table test) and improvement after training in patients' subjective rating of their visual impairments. (4) Stabilityofimprovements at the 3-month follow-up visit. (5) Return to part-time work in 20 (91%) of 22 patients. All mentioned results were significant (nonparametric tests; et level, .05; two-sided; adjusted for the number of tests).

Setting: Outpatients of a day clinic for the treatment of neuropsychological disorders that is associated with a city hospital. Patients: A consecutive sample of 22 hemianopic patients without neglect after unilateral stroke. Follow-up was possible in all cases. Interventions: Saccadic eye movement strategies were treated regularly (30-minute daily sessions 5 days per week; 25 to 27 total treatment sessions).

Conclusions: Training of compensatory eye movement strategies restores oculomotor functions, improves performance in functional visual activities, and reintegrates hemianopic patients into vocational life.

Main Outcome Measures: Visual perimetry results,

(Arch Neurol 1994;51:474-481)

H From the EKN Entwicklungsgruppe Klinische Neuropsychologie, City Hospital Bogenhausen, Munich, Germany.

OMONYMOUS VISUAL field defects (VFDs) are one of the most frequent consequences of brain damage.] Approximately 20% to 30% of all patients with cerebrovascular infarction requiring therapy in a rehabilitation center have homonymous VFDs.2 Among these, 70% show a visual field sparing of less than 5° of visual angle.1 Patients with VFDs have repeatedly been found to have a poor rehabilitation outcome, äs measured by analysis of activities of daily living (ADL), functional Status outcome indicated by the Barthel Index,3 or vocational rehabilitation success.4'5 In addition, Uzzell et al6 found that patients

ARCH NEURO17VOL 51, MAY 1994 474

with head trauma with VFDs exhibit more widespread neuropsychological defects than comparable patients without VFDs. Although other factors might also contribute to the unfavorable outcome of patients with VFDs in rehabilitation, it is surprising that VFDs have not been a major target for rehabilitation programs, äs has been the case for aphasia6-7 or visual neglect.8'10 Quantitative studies of vi-

See Patients and Methods on next page

PATIENTS AND METHODS PATIENTS Twenty-two patients with VFDs without visual neglect (16 male and six female) with a mean age of 46 years (ränge, 16 to 77 years) were included in the sample. Seven patients had left-sided homonymous hemianopia and 15 had right-sided hemianopia. All patients had a unilateral vascular brain lesion documentedby clinical (field defect) andneuroradiologic (magnetic resonance imaging) findings. Mean time after onset was 7.5 months (ränge, l to 37 months). None of the patients had hemiparesis. All patients underwent detailed neuropsychological examinations (for details, see von Cramon and Zihl 24 ). Patients with inadequate fixation during visual perimetry or visual search field testing and patients with oculomotor nerve palsies or central oculomotor disorders (see Leigh and Zee25) were excluded. All patients had normal function of the anterior visual pathways, äs evaluated by orthoptic and ophthalmologic tests (fundus and slit-lamp examinations). Corrected binocular visual acuity (Snellen letter chart) was at least 20/30 for the near (40-cm) and far (6-m) distances. All patients underwent detailed assessment of their visual complaints by a systematic questionnaire before and after visual training (see below). Patients with visual neglect were excluded from the study by testing horizontal line bisection and drawing of symmetrical figures from memory (for details, see Kerkhoff et al 11 ). Because patients with neglect deviate to the ipsilesional hemispace in horizontal line bisection26 and patients with VFDs deviate to the contralesional scotomatous hemifield,27'30 this deviation was taken äs one criterion to differentiate between patients with VFDs and those with neglect. All patients showed a displacement of the truncation point to the hemianopic hemifield beyond the cutoff scores. None of the 22 patients showed evidence of visual neglect in the drawing task.

white circular target (brightness, 102 candelas/m2) was chosen to determine the extent of the scotoma (for further details of perimetric measurement, see Kerkhoff et al11). Perimetric measurement accuracy was 0.45° within the central 15° of the visual field and 2.5° for the periphery, äs determined in our previous study. 11 VISUAL SEARCH FIELD Visual search field was measured with the Tübingen perimeter (for details, see Kerkhoff et al 11 ). The search field was defined äs the area in the perimeter (in degrees) that a patient could actively scan via eye movements but without head movements when searching for a bright, suprathreshold Stimulus. Insufficient compensation for a VFD will be reflected in time-consuming and small-amplitude saccades in the scotoma20 and hence a small visual search field (eg, the dashed line in Figure l , top). Alternatively, good oculomotor compensation for the VFD will result in a larger search field (eg, the dashed and dotted line in Figure l, top). The patient was required to fixate a small red spot in the center of the perimeter (diameter of the spot: 30 minutes of arc) of visual angle while the perimetrist moved the target (identical to that used during perimetry) with a velocity of approximately 2°/s from the periphery to the center of the sphere. The patient was instructed to search for the target by actively exploring the perimeter sphere using eye, but not head, movements. The patient rested his or her head on a chin rest, while bis or her forehead leaned against a supporting headband. The search field was measured 10 times along eight meridians; the sequence of the meridians was pseudorandom. For statistical analyses, we used the median of all search field values measured on the horizontal meridian located in the patient's blind field. Measurement accuracy of visual search field testing was 2.25° of visual angle (see Kerkhoff et al11 for details). Search field extension is 46° for each hemifield in healthy control subjects measured under exactly the same conditions.33

TESTS SEARCH ON PROJECTED SLIDES In designing the different measures of visual performance in our patients, we referred to the World Health Organization classification of levels based on which any disease may be analyzed (see Wade31)- These levels are pathology, impairment, disability, and Handicap. In this context, pathology is to be understood äs the underlying brain damage, impairment äs the resulting scotoma, disability äs the disorder of visual search and the accompanying visual problems (ie, bumping into obstacles) in daily life, and handicap äs the individual problems resulting from the disease (ie, loss of driver's license due to the scotoma). Pathology and handicap were not considered in this study.

We used three slides with geometric Symbols similar to the paper and pencil tests developed by Weintraub and Mesulam34 and nearly identical to the visual search test of Chedru et al.18 The patient sät 86 cm away from a white wall onto which slides were rear-projected that subtended 40° horizontally and 25° vertically. The patient had to indicate with a hand-held pointer all Symbols of a specific class (circles on slide l, triangles on slide 2, and squares on slide 3). The ratio of targets to distractors was held at approximately 50%. Omissions and multiple pointing to a target were rated äs errors.

VISUAL PERIMETRY

TABLE TEST

Binocular visual fields were mapped with a Standard Tübingen projection perimeter (Oculus, Wetzlar, Germany) .32 Eye position was monitored through a telescope. For kinetic perimetry, a large (diameter, 116 minutes of arc of visual angle)

The table test was designed to measure transfer of treatment strategies on nontrained visually related ADL. The patient was

ARCH NEUROL7VOL 51, MAY 1994 475

Continued on next page

seated in front of an 80X60-cm table containing 40 real objects randomly distributed on it (eg, pencil, eraser, coin, comb; Figure 2, top). The patient was shown an object and was asked to find the same object on the table äs quickly äs possible using eye and head movements but without changing his or her seatingposition. Search times were measured with a stop watch by the experimenter from the moment when the target object was shown to the patient. The table was invisibly divided into four quadrants of equal size. Within each quadrant, five objects had to be searched for while the other five served äs targets when the test was administered a second time (Figure 2, top). The sequence of the objects that the patient had to find was pseudorandom and thus unpredictable for the patient. For repeated measurements throughout the study, the table was rotated by 180° so that four different test versions were available (two kinds of targets, two orientations). Twenty healthy controls showed nearly identical search times for the same quadrant in each of the four versions. Search times of the different versions were significantly correlated (rbetween .93 and .98 for all four quadrants); the mean difference between any quadrant of the different versions was small (0.95 second; ränge, 0.1 to 2.0 seconds). No significant retest effect was seen. RATING OF SUBJECTIVE VISUAL IMPAIRMENT A questionnaire based on 11 items describing the most frequent visual impairments of patients with VFDs (eg, bumping into persons in the blind hemifield) was read to each patient before and after therapy. For each item, patients had to judge on a five-point scale to what extent they experienced the problem in question. The scale was äs follows: 0, no problem; l, rare problem; 2, partially relevant problem; 3, frequent problem; and 4, very frequent problem. The 11 items referred to in the "Results" section are shown in Figure 3. To minimize the tendency of the patients to answer in a socially desirable manner after therapy, they were not informed about their ratings at the beginning of therapy. TRAINING PROCEDURES Training procedures have been described in detail elsewhere. n The training comprised three major Steps: (l) performing large saccades to the blind field, (2) improving visual search on projected slides, and (3) transfer of both to ADL. During the first part of training, the targets were presented on a large Computer screen. The patient's task was to direct a large saccadic eye movement to the target shown in the blind field without head movements. Target onset was signaled acoustically. Target eccentricity, duration, predictability, and position within the patient's scotoma could be manipulated with the Software by the therapist. Improvement in saccadic training was checked regularly by measurements of the visual search field (see "Results"). Because patients with VFDs, like those with neglect,34 show disordered visual searching strategies in blind and intact field regions,18'19 the patients were then taught a systematic search strategy enabling them to scan the blind and

the intact visual fields without omission of relevant targets. A systematic scanning strategy (either horizontally row by row or vertically column by column) was demonstrated to the patient repeatedly, and he or she was encouraged to adopt one of these strategies when searching for targets on slides. In addition, all patients were urged always to begin their search in the periphery of their scotoma because this was the most likely area in daily living in which they would fail to notice persons or objects. Approximately 200 different slides were designed specifically for this stage of training.35 The slides varied according to the overall number and size of Stimuli, the target-foil ratio, the similarity among Stimuli, and systematic vs unsystematic spatial arrangement of Stimuli (rows and columns vs mixed). Improvement in visual search was measured with the test "search on projected slides." None of the slides used in the search on projected slides task were used for training. In the last part of the training, the patient was urged to use the scanning strategies in situations of everyday life. Application of the basic scanning strategies was trained directly in those situations that were rated äs being most problematic in the patient's individual Situation (eg, crossing a street). Possible improvements following this treatmentstep were evaluated by the table test and the subjective ratings of visual disabilities before and after therapy. Treatment sessions took place at least once daily for 30 minutes 5 days each week. Ten of the 22 patients received therapy in other areas, mostly memory training. Visual training lasted from 4 to 12 weeks, depending on the individual progress. Detailed therapy cutoff criteria were previously defined (see Kerkhoff et al 11 ). TREATMENT DESIGN All patients were treated in a baseline design to separate training-related improvements from possible effects of spontaneous recovery, adaptation to tests, and effects of medications or other therapies. Visual search field extension was defined äs the relevant target variable because it could be reliably and repeatedly measured in all patients with VFDs and has been shown to be a sensitive measure for the evaluation of the outcome of saccadic training in patients with VFDs.11 In addition, binocular visual fields were repeatedly measured before, during, and after training for the same reason. Measurements were performed weekly during therapy and three times before and after training (interval between each of the three measurements, at least l week) to establish a baseline period. Similarly, the table test was performed twice before training, directly after training, and once at follow-up to obtain baseline data. The search-on-slide test was administered directly before and after initiation of therapy and at follow-up (mean follow-up period, 3 months; ränge, l to 12 months). The subjective rating of disability was performed directly before and after training. Nonparametric tests were performed with an a level of .05 (two-sided). Adjustment of the a level in case of multiple pairwise comparisons was performed according to the Bonferroni procedure (see Holm36).

ARCH NEUROL7VOL 51, MAY 1994 476

sual field recovery11'14 suggest that some spontaneous recovery occurs in approximately 10% to 20% of patients and occurs within 2 to 3 months after brain damage in most cases. The extent to which visual fields can be recovered by systematic training, however, is controversial.12"16 At present, the majority of patients with VFDs probably have to face longterm visual problems associated with their VFDs14 because recovery of visual fields does not occur spontaneously or remains very limited even after extensive training.11>13>I5 This Situation has far-reachingconsequences for the ability of diese patients to adapt to vocational and private life. Poppelreuter17 and later researchers, using detailed eye movement recording techniques,18"20 have generally confirmed the view that patients with VFDs show disordered and slowed visual search in their blind hemifield. Consequently, they bump into obstacles, other persons, and door frames and collide with bicyclesor cars.1'21 Although a few studies have dealt directly with the restoration of visual field regions in patients with VFDs with rather limited success,2-12-16 the question äs to whether and how such patients can be successfully rehabilitated using compensatory mechanisms is completely open. It is not known whether systematic training in patients with VFDs leads to a transfer of training effects to visually related ADL, which is one of the major aims of cognitive rehabilitation.22 In a recent study,1 * we were able to show that saccadic compensation training leads to a significant improvement in visual search in patients with homonymous VFDs and patients with additional left-sided visual neglect. However, because that study employed a design whereby visual search was measured before and after training and during a follow-up period, treatment-related gains in visual performance could have been influenced by factors not related to treatment. Furthermore, the transfer of these improvements to visually related ADL was not addressed in that study. Finally, the patients' subjective experience of their visual impairments was not assessed throughout therapy. Because the transfer of treatmentrelated gains is one of the major aims of cognitive rehabilitation22 and is unlikely to occur on its own, it is necessary to demonstrate that the therapy in question leads to measurable improvements in relevant outcome measures. However, most of the available outcome scales score visual performance on a very coarse level and are too nonspecific to measure therapeutic changes.23 Therefore, new, sensitive measures had to be designed to evaluate the transfer of treatment gains. The present study was planned to evaluate the following questions in the rehabilitation of patients with VFDs: (1) What is the relative contribution of restitution of function (field recovery) vs acquisition of compensatory strategies (systematic scanning within the scotoma)? (2) Does systematic treatment of patients with VFDs and their visual problems lead to a transfer of training-related improvements in visual ADL? Do improvements remain stable during long-term follow-up after cessation of training? (3) Do treated patients experience

Baseline

Treatment

Follow-up

5 6 7 No. of Sessions

10

4540353025201510-

4

11

Figure 1. Top, Demonstration of a typical visual search field border in a patient with a left-sided homonymous hemianopia before training (dashed line) and after training (dashed and dotted line). Bottom, Visual search field size in the scotoma (in degrees of visual angle) at baseline and during treatment and follow-up in 22 patients with unilateral visual field defects. Vertical bars indicate SEs.

subjectively the observed improvements in visual performance after therapy? RESULTS

RESTITUTION OF VISUAL FIELD Only visual field increases surpassing measurement error were considered valid. Partial restitution of visual field during systematic visual treatment was observed in 12 (54%) of 22 patients (Table l). Friedman analyses of ranks for dependent data37 showed a significant difference between the measurement dates(x 2 =22.18, P=.0001). Pairedcomparisons with Wilcoxon tests revealed a significant visual field increase only during training from the second pretest to posttest measurement (z=3.29, d/=2, P=.001). No other comparisons reached statistical significance (smallest P=.20). Actual visual field increase was less then 8° in nine of the 12 patients with enlarged visual fields after training. However, the three remaining patients showed considerable increases of 11°, 17°, and 24° along the measured meridian.

ARCH NEUR017VOL 51, MAY 1994 477

O

A

o o

o o A

A

o

o! A

A l

A! o i

A

o

O

c)

Notice Obstacles

o

O A

IV linimum

Bump Into Obstacles

c) A o A

A

0

1.0 1.5 2.0 2.5

^^m

3.0

Maximum 3.5 4 0

i



1

• M

0 A

0.5

Using Public Traffic

o



, ... l



Finding Way in Clinic ^m Find Therapist's Boom , • Find Way at Home •... Crossing Street •

' i i •. |

Figure 3. Mean ratings of subjective disability/visual prob lern s resulting from the scotoma betöre (shaded bars) and after (black bars) visual training in 22 patients with visual field defects. See "Patients and Methods" section for an explanation of the scale. Cutoft for Healthy Controls Upper Scotoma

Lower Upper Scotoma Intact Table Test

Lower Intact

Figure 2. Top, Outline of the table test. P indicates patient; dotted lines, the quadrants of the test, which are invisible to the patient; triangles, targets A; and circles, targets B. Bottom, Mean search times for the table test at two baseline measurements before treatment (pretreatment 1 and pretreatment 2), after treatment, and at follow-up in 22 patients with visual field defects. Dashed line indicates mean+2.5 SDs of performance of 20 healthy controls in this task; vertical bars, SEs.

VISUAL SEARCH FIELD Figure l shows the results of the visual search field measurements during the baseline, treatment, and follow-up phases for all patients. Friedman tests revealed no significant difference in search field size in the scotomatous field region between the three baseline measurement dates (x2=3.025, d/=2, P=. 2204). As can be seen in Figure l, search field values ranged between 10° and 20° before training and were thus severely reduced compared with normal values (46°). During treatment, a significant improvement was seen in visual search field size (Friedman test: x2=52.18, d/=4, P=.0001). To reduce the number of statistical comparisons, only the last baseline measurement and the last measurement during training were compared (Wilcoxon Test). A significant improvement in search field size was seen between these two measurements (e=3.91, P=.0001). After cessation of visual training, while other therapies (eg, memory training) still continued in 10 of the 22 patients, no significant change was seen compared with the last treatment measurement (^=.24, P=.40). During follow-up, the search field values remained stable, ie, no further improvement or any significant decrease in visual search field size was seen (Friedman test: x2= l -02, df=2, P=.59). In addition, the patients with VFDs scored signifi-

cantly better on any follow-up measurement compared with any of the baseline measurements (all P.05 for both hemifields). A similar reduction in overall search time on the three slides was seen (Friedman test: x2=21.94,P=.0001). Paired comparisons showed a significant reduction from pretreatment to posttreatment measurements (^=3.01, P=.001) but no further significant change compared with follow-up (^=1.16, P>.05). In summary, the patients performed more accurately and quickly in visual search on projected slides after training than before, although they were still impaired in relation to the healthy controls. TABLE TEST No significant improvement in search time was seen in any of the four quadrants of the table test between the first and second pretests (Figure 2, smallest P=.25). Friedman tests

ARCH NEUR017VOL 51, MAY 1994 478

Table 1. Mean Visual Field Sparing Betöre and After Visual Training and at Follow-up and Mean Visual Field Increase in 22 Patients With Visual Field Defects Condition

Table 2. Results of the 'Search on Projected Südes' Test in 10 Controls and 22 Patients With Visual Field Defects Before and After Treatment and at Follow-up After Treatment

Mean (Range), Degrees Condition

Pretest

Mean (Range)

Mean increase

4.7(1-13) 4.9(1-13) 7.9(1-30) 8.0(1-30) 3.0 (0-24)

Errors, blind field

Mean increase of patients with partial field recovery (n=12)

Before treatment

2.7 (0-27)

6.6 (2-24)

After treatment

0.7(0-12)

Follow-up

0.6 (0-10)

1 2

After therapy At follow-up

4.6 (0-27) 0.8(0-11) 0.7 (0-10)

Before treatment After treatment Follow-up Errors, intact field

Overall search time, s

revealed a significant difference between pretreatment, posttreatment, and follow-up measurements for the upper scotomatous quadrant (x2=26.46, d/=3, P< .0001), for the lower scotomatous quadrant (x2=19.76, d/=3, P.30). The last result was due mainly to large variances. N o significant change was seen between posttreatment and follow-up measurements in any of the quadrants (smallest P=.30). As can beseen in Figure 2, bottom, the 22 patients with VFDsshowed a nearly 50% reduction in search time after training but no change after cessation of treatment and follow-up. RATING OF SUBJECTIVE DISABILITY Figure 3 shows the ratings of the mean subjective disability before and after visual training. In all items, significant improvements during therapy were reported by the patients (Wilcoxon tests, largest P=.001). TREATMENT VARIABLES Patients with left-sided homonymous VFDs received 27.3 (ränge, 18to40) treatment sessions, while those with rightsided homonymous VFDs received 25.5 (ränge, 10 to 65) sessions. This difference was not statistically significant (17=54, P>.05). Time after onset, side of field defect, age, and sex were not correlated to recovery of performance in any of the visual tests (P>.30 in all correlations). LEFT VS RIGHT HEMIANOPIA Patients with left-sided and right-sided homonymous VFDs differed in visual field sparing before training (U test: 17=21, P=.025, corrected for ties) and after training (17=21, P=.025, corrected for ties); however, no differences were found between the two groups regarding the size of the visual search field before, during, or after training (smallest P=.09) or search times in the table test and during search on projected slides (smallest P=.26). Furthermore, no difference was seen in subjective ratings (smallest P=. 20), except that right-sided

Before treatment

96.2 (50-130)

After treatment

75.8 (44-90)

Follow-up

74.4(41-87)

Controls, overall search time

55.4 (35-60)

Controls, errors on left/right

0.5 (0-2)/0.4 (0-2)

hemianopics reported bumping into obstacles on their right side and left-sided hemianopics on their left side. Furthermore, the groups did not differ in visual field gain during training (17=49.5, P=.81),nordidtheydiffer in visual search field gain throughout treatment (U=24, P= l .0). In summary, left-sided and right-sided hemianopics performed entirely similarly, except for the difference in field sparing, and there was no evidence that left-sided hemianopics performed like patients with left-sided visual neglect. LOCATION OF LESION The location of lesions was rated according to the radiologic findings äs predominantly occipital (n= 12), predominantly temporal (n=7), or occipitotemporal (n=3). Neither visual field gain throughout treatment (Kruskal-Wallis test: x2= l -02, P=.59) nor visual search field gain (x2=5.01,P=.08) differed among these three groups. The same was found for the reduction in search time in the table test (x2=.53, P=.77), for the search on projected slides (x2=3.11, P=.21), and regarding the number of treatment sessions (x2=2.91, P=.23). Hence, there was no evident relationship between location of lesion and performance during training. However, it should be mentioned that lesion size was not taken into account due to the varying optical quality of the computed tomographic and magnetic resonance imaging scans. EARLY VS LATE TRAINING To test whether early vs late training after brain damage had any differential outcome, we performed a median split of the total sample (median of 6 months for time after onset) and compared improvement on all tests, except for the subjective ratings. No significant differences were found between the two groups in any of the comparisons (smallest

ARCH NEURO17VOL 51, MAY 1994 479

P=.20). Inaddition,impairment in visual performance was not significantly correlated to time after onset, sex, or cause (Pearson correlation: largest r=.20 [notsignificant]). RETURN TO WORK Twenty of the 22 patients with unilateral VFDs returned to work after their rehabilitation. All patients returned to their previous Job, but 15 worked only part-time. COMMENT

The efficacy of cognitive rehabilitation in stroke victims and those surviving traumatic brain injury has been repeatedly debated in recent years because of its growing prevalence and thus the increasing bürden that care and rehabilitation of these patients impose on society 22,31,38-42 jo our k now i e dg ei our study is the first to combine stringent baseline methods with a group design in a larger sample of patients with VFDs than typically reported in most single case studies.43 Before discussing our results, we will consider relevant methodologic issues. First, a randomized control group design has been advocated in most critiques of the present state of the art in cognitive rehabilitation.38 While these designs may have some advantages, especially when the patients under study remain in the clinic for only a limited time so that baseline designs are difficult to implement, they have two clear disadvantages: (1) they require large, homogeneous patient groups and (2) they normally require at least two equally promising treatment approaches because allocation to a nontreatment group or nonoptimal treatment group is ethically complicated. We chose the combination of a baseline design within a larger patient group because our patients remained in the clinic sufficiently long to allow for baseline and follow-up measurements, and a second wellestablished treatment technique, such äs visual search field training,11 was not available. In addition, strictly parallel subgroups are extremely difficult to establish. Another possible explanation for the observed improvements could be simply a placebo effect. This argument cannot be discarded easily, äs we had no untreated control group for ethical reasons. However, there is pertinent evidence from our previous work.11 We measured two untreated visual covariables throughout the study in some patients to monitor the specificity of improvements after search field training. We found virtually no improvement in performance in five patients with disturbed light or dark adaptation throughout search field training. Moreover, two patients with severely disturbed visual object identification showed no improvement in this ability, while they improved dramatically in visual search field size during training. In summary, the specificity of improvements in visual search while other untreated visual deficits remained unchanged throughout the course of the study strongly argues against the nonspecific placebo

effect's being responsible for the observed improvements. As an aside, it is difficult to explain why the improvements in visual search field clearly coincide with treatment onset. With these considerations and caveats in mind, our results show that measurement variability, adaptation to test procedures, or spontaneous recovery cannot explain the fact that the gains in any of the measures clearly coincided with treatment onset and ranged far beyond any test-retest effect, äs seen from the baseline measurements and the results from the healthy controls. Placebo effects cannot be ruled out entirely but seem unlikely, given the specificity of improvements. Furthermore, most of our patients with a mean time after onset of 7.5 months clearly had more chronic disease, which renders spontanous recovery even more unlikely. Stability of improvements could be demonstrated in follow-up examinations l to 10 months later in all tests. No difference was found between patients receiving "early" vs "late" visual training after their brain damage, äs has been shown for aphasia rehabilitation. 7 This implies that visual rehabilitation in our patient group improves compensatory saccadic eye movements even in patients with a time after onset of more than l year. Left-sided vs right-sided hemianopics did not differ regarding their improvements, although the latter group showed additional visual field sparing. This may indicate that disorders of visual search are equally distributed in left-sided and right-sided hemianopic patients when there is no evidence of additional neglect. Furthermore, it means that both left-sided and right-sided hemianopics are good candidates for training of visual search. Lesion location did not have a differential effect on training success. However, patients with neglect were excluded so that no patients in our sample had parietal lesions. With regard to the two aims of our study, we found significant training-related improvements of saccadic eye movement strategies in all trained patients, which may indicate that training of compensatory techniques to cope with the disability in daily life seems to be a very promising form of neurovisual rehabilitation. In contrast, recovery of scotomatous field regions during therapy was achieved in 12 of 22 patients but was quantitatively rather limited compared with the large improvements in visual search field. Morover, a priori prediction concerning in which patients and to what extent visual fields would recover would have been impossible from our data. This problem could possibly be overcome by using positron emission tomography to indicate in which patients systematic training could restore damaged field regions (see Bosley et al44). Because transfer of treatment gains to daily life is not likely to happen spontaneously, we incorporated this äs a last Step in our treatment program and designed new measures to evaluate possible improvements. The results showed significant transfer effects of training in the table test, indicating that the training of saccadic compensatory eye movement strategies ameliorates the relevant visual problems in daily life resulting from the sco-

ARCH NEUR01WOL 51, MAY 1994 480

toma, such äs finding objects on a table. The results of the table lest show another interesting effect: head movements are not suitable to compensate for the deficits in visual search in patients with VFDs, äs can be seen from the deficient performance in the table test during the baseline measurements despite free head movements. The subjective improvements noted by the patients are quite impressive even if one attributes part of the improvement to the patient's tendency to give socially desirable answers to the therapist. Alternatively, the reduced scores on the questionnaire after training might indicate reduced awareness of the visual problems in our patients after training. This is extremely unlikely because information about daily visual problems resulting from the scotoma and use of compensatory scanning strategies was part of each training session. Moreover, successful return to work (in 20 of 22 cases) would not have occurred in patients who were unaware of their visual problems. Our study demonstrates that systematic training of compensatory strategies in patients with VFDs without neglect leads to significant improvements in basic oculomotor functions. The observed transfer to visually related ADL, the patients' subjective improvements in their visual impairments, and the return to work in 91% of patients demonstrate clearly the efficacy of the present treatment approach in visual neurorehabilitation. Accepted for publication May 17, 1993. We are grateful to Elisabeth Stögerer, Elisabeth Haaf, Gisela Eberle-Strauss, and Gabriele Ramgraberfor treatments; Charles Heywood, PhD, for improving the style ofthe manuscript; and two anonymous reviewers of the manuscript. Reprint requests to EKN Entwicklungsgruppe Klinische Neuropsychologie, City Hospital Bogenhausen, Dachauer Str 164, D-80992 Munich, Germany (Dr Kerkhoff). REFERENCES 1. Zihl J. Cerebral disturbances of elementary visual functions. In: Brown JW, ed. Neuropsychology of Visual Perception. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988. 2. Rossi PW, Kheyfets S, Beding MJ. Fresnel prisms improve visual perception in stroke patients with homonymous hemianopia or unilateral visual neglect. Neurology. 1990:4:1597-1599. 3. Reding MJ, Potes E. Rehabilitation outcome following initial unilateral hemispheric stroke: life table analysis approach. Stroke. 1988:19:1354-1358. 4. Groswasser Z, Cohen M, Blankstein E. Polytrauma associated with traumatic brain injury. Brain Inj. 1990:4:161-166. 5. Savir H, Michelson l, David C, Mendelson L, Najenson T. Homonymous hemianopsiaand rehabilitation in fifteen cases of CCI. Scand J RehabilMed. 1977:9:151-153. 6. Uzzell BP, Dolinskas CA, Langfitt TW. Visual field defects in relation to head injury severity: a neuropsychological study. Arch Neurol. 1988:45:420-424. 7. Wertz RT, Weiss DB, Aten JL, et al. Comparison of clinical, home and deferred language treatment for aphasia. Arch Neurol. 1986:43:653-658. 8. Weinberg J, Diller L, Gordon WA, et al. Visual scanning training effect on readingrelated tasks in acquired right brain damage. Arch Phys Med Rehabil. 1977; 58:479-486. 9. Robertson l, Gray J, McKenzie S. Microcomputer-based cognitive rehabilitation of visual neglect. Brain Inj. 1988:2:151-163. 10. Robertson l, Gray J, Pentland B, Waite LJ. A randomized controlled trial of computer-based cognitive rehabilitation for unilateral left visual neglect. Arch Phys Med Rehabil. 1990:87:236-242.

11. Kerkhoff G, Münßinger U, Haaf E, Eberle-Strauss G, Stögerer E. Rehabilitation of homonymous scotomata in patients with postgeniculate damage of the visual system: saccadiccompensation training. Restorative Neurol Neurosci. 1992:4:245-254. 12. Zihl J, von Cramon D. Restitution of visual function in patients with cerebral blindness. J Neurol Neurosurg Psychiatry. 1979:42:312-322. 13. Zihl J, von Cramon D. Visual field recovery from scotoma in patients with postgeniculate damage. Brain. 1985;108:439-469. 14. Zihl J, von Cramon D. Recovery of visual fields in patients with postgeniculate damage. In: Poeck K, Freund HJ, Gänshirt H, eds. Neurology. New York, NY: Springer-Verlag NY Ine; 1986:188-194. 15. Potthoff RD. Partial visual field rehabilitation in two various cases of homonymous hemianopia. Eur J Neurosci Suppl. 1988:73:10. Abstract. 16. Balliet R, Blood KMT, Bach-y-Rita P. Visual field rehabilitation in the cortically blind? J Neurol Neurosurg Psychiatry. 1985:48:1113-1124. 17. Poppelreuter W. Die psychischen Schädigungen durch Kopfschuß im Kriege 1914/1916. Vol l: Die Störungen der niederen und höheren Sehleistungen durch Verletzungen des Okzipitalhirns. Leipzig, Germany: Voss; 1917. 18. Ch6dru F, Leblanc M, Lhermitte F. Visual searching in normal and braindamaged subjects. Cortex. 1973:9:94-111. 19. Ishiai S, Furukawa T, Tsukagoshi H. Eye-fixation patterns in homonymous hemianopia and unilateral spatial neglect. Neuropsychologia. 1987:25:675-679. 20. Meienberg 0, Zangemeister WH, Rosenberg M, Hoyt WF, Stark L. Saccadic eye movement strategies in patients with homonymous hemianopia. Ann Neurol. 1981:9:537-544. 21. Williams D, Gassei MM. Visual function in patients with homonymous hemianopia, l: the visual fields. Brain. 1962:85:175-250. 22. Levin HS. Cognitive rehabilitation. Arch Neurol. 1990:47:223-224. 23. Mai N. Evaluation in constructing neuropsychological treatments. In: von Steinbüchel N, von Cramon DY, Pöppel E, eds. Neuropsychological Rehabilitation. New York, NY: Springer-Verlag NY Ine; 1992:96-99. 24. von Cramon D, Zihl J. Neuropsychologische Rehabilitation. New York, NY: SpringerVerlag NY Ine; 1988. 25. Leigh RJ, Zee DS. The Neurology of Eye Movements. San Francisco, Calif: Davies; 1983. 26. Heilman KM, Watson RT, Valenstein E. Neglect. In: Fredericks JAM, ed. Handbook of Clinical Neurology. Vol 1: Clinical Neuropsychology. Amsterdam, the Netherlands: Eisevier Science Publishers; 1985. 27. Axenfeld D. Eine einfache Methode: Hemianopsie zu constatieren. Neurol Zentralbl. 1894:13:437-438. 28. Liepman H, Kalmus E. Über eine Augenmasstörung bei Hemianopikern. Berl Klin Wochenschr. 1900;3:838-842. 29. Kerkhoff G. Displacement of the egocentric visual midline in patients with altitudinal postchiasmatic scotomata. Neuropsychologia. 1993:31:261-265. 30. Schenkenberg T, Bradford TC, Ajax ET. Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology. 1980;3:509-517. 31. Wade DT. Neurological rehabilitation. In: von Steinbüchel N, von Cramon DY, Pöppel E, eds. Neuropsychological Rehabilitation. New York, NY: SpringerVerlag NY Ine; 1992. 32. Aulhorn E, Harms J. Visual perimetry. In: Jameson D, Hurvich L, eds. Handbook of Sensory Physiology. New York, NY: Springer-Verlag NY Ine; 1972;7:102-145. 33. Zihl J, von Cramon D. Zerebrale Sehstörungen. Stuttgart, Germany: Kohlhammer Verlag; 1986. 34. Weintraub S, Mesulam MM. Visual hemispatial inattention: Stimulus Parameters and exploratory strategies. J Neurol Neurosurg Psychiatry. 1988:5:1481-1488. 35. Münßinger U, Kerkhoff G. Therapy for disturbed visual search in patients with postchiasmatic visual field disorders and visual neglect. In: EKN Materialien für die Rehabilitation. Dortmund, Germany: Borgmann Publishing; 1994. 36. Holm S. A simple sequentially rejective multiple test procedure. Scand J Stat. 1979:6:65-70. 37. Siegel S. Nichtparametrische Statistische Methoden. Frankfurt am Main, Germany: Verlagsbuchhandlung, Verlag für Psychologie; 1976. 38. Reding MJ, McDowell FH. Focused stroke rehabilitation programs improve outcome. Arch Neurol. 1989:46:700-701. 39. Dobkin BH. Focused stroke rehabilitation programs do not improve outcome. Arch Neurol. 1989;46:701-703. 40. Hachinski V. Stroke rehabilitation. Arch Neurol. 1989:46:703. 41. Berrol S. Issues in cognitive rehabilitation. Arch Neurol. 1990:47:219-222. 42. Volpe BT, McDowell FH. The efficacy of cognitive rehabilitation in patients with traumatic brain injury. Arch Neurol. 1990;47:220-222. 43. Gianutsos R, Matheson P. The rehabilitation of visual perceptual disorders attributable to brain injury. In: Meier MJ, Benton AL, Diller L, eds. Neuropsychological Rehabilitation. New York, NY: Churchill Livingstone Ine; 1987. 44. Bosley TM, Rosenquist AC, Kushner M, et al. Ischemic lesions of the occipital cortex and optic radiations: positron emission tomography. Neurology. 1985;35:470-484.

ARCH NEUR017VOL 51, MAY 1994 481

Suggest Documents