Ординатура / Офтальмология / Английские материалы / The Neuropsychology of Vision_Fahle, Greenlee_2003

322 JOSEF ZIHL

of the visual pathway which contains the foveal fibre connections to the striate cortex. Complete destruction of both retrogeniculate pathways results in total cerebral blindness. Figure 11.1 shows examples of the main homonymous field disorders. Table 11.2 gives details on the incidence of the different types of visual field loss. Homonymous hemianopia is the most frequent type (65%) of field loss, followed by quadranopia and paracentral scotomata. The fovea is always spared, but the degree of parafoveal sparing can vary; in the majority of patients (~75%) it is less than 5 (Zihl 2000).

Apart from the loss of all visual functions in one hemifield, as for example in hemianopia, vision may be degraded (amblyopia), or visual perceptual functions may be selectively lost in one hemifield. Selective hemianopias have been reported for colour (hemiachromatopsia; Paulson et al. 1994), form (Frassinetti et al. 1999), and movement (Plant et al. 1993; Schenk and Zihl 1997). Thus, the representation of the visual field exists also beyond the striate cortex, i.e. in extrastriate visual cortical areas, for stimulus dimensions other than light vision.

Spatial contrast sensitivity (‘visual blurring’), visual acuity, and visual adaptation

Spatial contrast sensitivity and visual acuity can be impaired after either unior bilateral retrogeniculate injury (Hess et al. 1990) with pronounced reduction in visual acuity being mainly reported after bilateral injury (Frisén 1980). Spatial contrast sensitivity and visual acuity can be dissociated when single optotypes are used to assess visual acuity. Visual adaptation can also be affected after retrogeniculate injury. Patients may show either reduced light or dark adaptation, or both (Zihl and Kerkhoff 1990).

Colour vision

This can be impaired either in one hemifield (hemiachromatopsia) and partly in the fovea after leftor right-sided injury to the lingual and fusiform gyri, or can be impaired (cerebral dyschromatopsia) or lost (cerebral achromatopsia) in the entire hemifield when these structures are damaged in both hemispheres (Damasio et al. 1980; Paulson et al. 1994). Some patients also exhibit impaired selective colour constancy (Ruttiger et al. 1999).

Disorders in orienting in and exploring of visual space

These refer to impaired visual spatial abilities (e.g. inaccurate visual localization, deviation of visual vertical, horizontal, and straight-ahead axes, defective depth perception and stereopsis, visual spatial orientation), spatial knowledge concerning the actual or virtual (mental) environment, and restriction of spatial attention (visual neglect, Balint’s syndrome; see below). Such disorders are common after occipitoparietal and posterior parietal injury, with a right-hemisphere damage more frequently causing deficits (for comprehensive reviews, see De Renzi 1982; Grüsser and Landis 1991; Karnath and Zihl 2001).

324 JOSEF ZIHL

Table 11.3 Effects of visual deficits on visual performance

that especially visual overview and visual orientation, visual identification and recognition, and reading can be impaired not only when the underlying visual capacities and abilities are impaired themselves (e.g. visual space perception, visual cognition), but also when crucial prerequisites (e.g. visual field, contrast sensitivity and visual acuity, visual spatial attention) are affected.

Spontaneous recovery of cerebral visual disorders

Visual field disorders

Spontaneous recovery of vision in patients with anopia has been frequently reported; it typically takes place within 2–3 months postinjury. The frequency and amount of recovery appears, however, to be limited. About 15% of patients may show recovery of visual field in the range of 3–24 degrees, with an average of about 5 degrees (Zihl 2000). In only 4 of 225 patients ( 2%) was complete recovery observed. Recovery from complete cerebral blindness also may take place within 8–12 weeks after the onset of blindness; however, in some cases it can last for up to 2 years. About 30% of 111 patients reported in the literature showed recovery. In four of them complete return of vision was observed. In the rest recovery ranged from a return of ‘crude’ light vision to recovery of visual field portions with or without colour and form vision. Typically vision returns first in the

RECOVERY AND REHABILITATION OF CEREBRAL VISUAL DISORDERS 327

function in question, which does not show any recovery at all, or returns only to a limited degree, does return during or after a period of practice specifically addressing this deficit. In the case of elementary and thus rather well defined visual functions, e.g. visual field, spatial contrast sensitivity, visual spatial abilities, or colour vision, training procedures can be developed that may specifically influence these functions. In contrast, in the case of complex visual capacities, e.g. visual orientation, visual identification and recognition, or visual spatial attention, the demonstration of recovery appears more difficult, because the underlying neural network consists of several components. In an individual patient showing a complex visual disorder, it may be impossible to entangle these different components and to decide which one(s) is (are) affected, and which spared, or which component should be improved first. This difficulty is even more pronounced in patients with a combination of elementary and complex visual deficits. This may explain why little experimental evidence is available especially on recovery of complex visual capacities after training. There is no proven golden rule as to how to proceed, but a reasonable and successful guideline may be to compose appropriate methodology and knowledge about the functional organization of the brain in general, and the visual brain in particular. In addition, it appears especially useful to consider basic rules of perceptual learning (Zihl 2000; Fahle and Poggio 2001). In this context a sensible heuristic tool is to predict the outcome on the basis of the known interdependencies and interactions of elementary and complex visual capacities. If, for example, in a patient with paracentral visual field loss or reduced contrast sensitivity, reading is impaired, then this impairment can either be explained by the visual field loss or by the reduction in contrast sensitivity. If the first assumption is correct, then reducing the impairing factor (i.e. the visual field loss) should lead to an improvement in reading without further training. If the second assumption holds true, then training of spatial contrast sensitivity is required. A similar consideration may be helpful when confronted with a complex disorder. For example, a patient’s difficulty in visually recognizing objects may result from defective selection of features that characterize certain objects, or defective integration of several object features into a gestalt, or both (which may be difficult to diagnose). The training of selection procedures should lead to recovery of this complex visual ability only if selection is impaired. Otherwise, either feature integration has to be trained, or both selection and integration require specific practice.

Visual field deficits

Visual field loss has attracted the most research interest. One possible reason for this is that highly valid and reliable quantitative methods are available to measure this visual deficit. Another reason is that comparable visual field defects have been produced in primates, and spontaneous recovery as well as recovery by systematic practice have been studied in detail (Cowey and Weiskrantz 1963; Mohler and Wurtz 1977). Thus, there was substantial support for the assumption that vision may also recover in anopic field regions in humans when we (Zihl and von Cramon 1979; Zihl 1981)

328 JOSEF ZIHL

(a)

(b)

Fig. 11.3 Visual field recovery after systematic practice with saccadic eye movements in two patients showing unilateral occipital stroke. (a) In this 54-year-old patient the visual fields (1) were taken 8 weeks after the stroke; no spontaneous recovery was observed during this period. After 280 trials (2) vision returned (hatched area) in the right upper quadrant. (b) In this 66-year-old patient the visual fields (1) were taken 13 weeks after the stroke; no spontaneous recovery was observed during this period. After 340 trials (2) vision returned (hatched area) in the left lower quadrant. For both patients vision in the peripheral parts remained depressed.

presented the first empirical evidence. The methods of training were based on experimental work in primates, and consisted of a close link between visual attention focused on the field region subjected to practice, and the detection or saccadic localization of a light target presented at the visual field border or within the anopic region. The patient had either to indicate the presence of the target or to shift the gaze to that position in the anopic field region where he guessed that the target may have appeared. In the latter condition, presentation time was always shorter (100 ms) than saccadic latency. Patients were never informed about the correctness of their response. Figure 11.3 shows examples of visual field recovery. Interestingly, visual field recovery was only observed in periods of training and not in intervals without training. Thus recovery was strongly linked to specific practice and did not result, e.g. from delayed spontaneous recovery. In addition, not only light but also colour and form vision returned in many patients indicating that visual information could be conveyed again to exstrastriate visual cortical areas not affected by the lesion.

The explanation that recovery was found in some but not in all patients was based on the assumption that recovery may only take place in patients with reversible neuronal loss and sparing of function—the work of Bosley et al. (1987) supports this idea. Since, in our patients, the time elapsed between the onset of the hemianopia and the onset of specific training varied between 1 and 28 months, a further assumption is needed to

RECOVERY AND REHABILITATION OF CEREBRAL VISUAL DISORDERS 329

explain recovery. Visual cortical neurons may have survived at the border zone of the lesion but may still not (fully) be engaged in visual processing. Although this issue has not been studied systematically, there is evidence that this hypothesis might be valid. Spontaneous and training-induced recovery of visual field regions has been reported even 16 and 28 months postonset, respectively (Zihl and von Cramon 1985; Poggel et al. 2001). In addition, visual field recovery was only found in patients with some sparing of light vision at the border between the intact field and the blind field. In this zone, thresholds for light detection were found to be particularly sensitive to attention (Zihl and von Cramon 1979). These observations may be taken as evidence that the transition zone may indeed represent residual neuronal function that can be modulated by attentional processes (Zihl and von Cramon 1985). Some authors have confirmed these results using similar methods of practice (Kerkhoff et al. 1992a,b; van der Wildt and Bergsma 1997; Kasten et al. 1998, 2000), but others have not (Balliett et al. 1985; Pommerenke and Markowitsch 1989). One main reason for the negative findings lies certainly in the (incorrect) assumption that every patient demonstrating a homonymous visual field defect also shows recovery of vision after training. As pointed out, only patients with spared neuronal activity in the striate cortex can be expected to do so (Zihl and von Cramon 1985). Thus, ‘local plasticity’ in terms of spared neurons (‘silent neurons’) surviving the injury does not exist in all patients and, without plasticity, no recovery of vision can be expected (Potthoff 1995; Sabel 1999; Kerkhoff 2000).

Although the results on recovery of visual field from scotoma look very promising, their behavioural significance remains to be examined. Rehabilitation first of all signifies a reduction in the degree of handicap in everyday life. In the case of visual field loss this should imply expanded view over the surroundings, fast and reliable detection of stimuli in all regions of the visual field, and normal reading performance. Thus, visual field enlargement has to reach a certain degree; otherwise it does not reduce the patient’s disability. For normal reading performance, at least 5 in the left and 6–7 in the right hemifield are required (Zihl 1995b). For a sufficient overview, at least a field extent of 20 on either side is required; otherwise visual orientation and navigation remain impaired (Lovie-Kitchin et al. 1990). Admittedly, only a very small number of patients (6 of 44, or 14%) had a visual field with a size of at least 20 after training. The number of patients with at least 5 on the affected side of the fovea was larger (15 of 32, or 47%); these patients showed significantly improved reading after training (Zihl and von Cramon 1985).

Spatial contrast sensitivity

There is preliminary evidence that spatial contrast sensitivity can be improved after systematic training of spatial resolution. Practice with discrimination of spatial frequencies not only increases contrast sensitivity, but is associated with an increase in visual acuity and reading performance (Zihl 2000).

330 JOSEF ZIHL

Colour vision

Perception of colour hues in patients with severely impaired foveal colour vision can be improved by systematic practice with hue discrimination (Zihl 2000).

Visual spatial capacities

Specific practice with position and distance estimation, discrimination of line length and line orientation, and discrimination of spatial axes has been reported to represent an effective means for recovery of these spatial abilities at least in some patients (Lütgehetmann and Stäbler 1992).

Visual agnosia

The first evidence of successful treatment of visual agnosic patients was presented by Poppelreuter (1917/1990). In a more recent attempt (Zihl 2000), the essential prerequisites for identifying and recognizing complex visual stimuli were trained in two patients with severe visual agnosia for objects, faces, scenes, and letters. Specific practice procedures included processing and selection of relevant features, and the use of cognitive strategies to supervise and control these processes. After training, both patients showed a significant improvement in visual identification and recognition (including naming) for all stimulus categories used in practice, but one patient still showed prosopagnosia. Thus visual agnosia may also show recovery and patients may regain, at least in part, the ability to visually recognize stimuli.

Visual neglect

Since the main symptom of visual spatial neglect is an absent or at least reduced exploration of contralesional space, the main treatment is based on procedures to direct orientation towards this side. These procedures aim to enlarge the field of attention in the affected hemispace and thus enhance exploration towards this side by training the patient to perform eye or hand movements to the impaired side. In this way, contralesional shifts of attention and visual exploration are improved (for a review, see Karnath and Zihl 2001). Because of the widespread neural network subserving visual spatial attention and visually guided activities in space (e.g. Mesulam 2000), it is not entirely clear whether the effect can be interpreted as recovery from visual neglect or as circumvention of the underlying visual-attentional disorder by learning compensatory strategies. In functional terms, the return of attention and of visually guided oculomotor and hand motor activities in the affected hemispace can certainly be understood as recovery.

Balint’s syndrome

In three patients suffering from severe Balint’s syndrome, specific practice with the initiation and execution of gaze shifts, with shifting attention and fixation to stimuli outside the actual field of attention, and reaching or grasping for them resulted in an enlargement of the field of attention and of the range of oculomotor and handmotor

RECOVERY AND REHABILITATION OF CEREBRAL VISUAL DISORDERS 331

Fig. 11.4 Oculomotor scanning patterns (infrared eye movement recordings) during inspection of a scene. (a) A 42-year-old normal subject (scanning time, 12.8 s). (b) A 53-year-old patient with left-sided hemianopia (field sparing, 3 ) and spontaneous adaptation to the field loss (scanning time, 13.4 s). (c), (d) A 47-year-old patient with left-sided homonymous hemianopia (field sparing, 3 ) without spontaneous adaptation (c) before (scanning time, 26.5 s) and

(d) after (scanning time, 11.4 s) specific practice with visual scanning. x-axis, horizontal extension of stimulus field (40 ); y-axis, vertical extension (32 ). 0, Centre; negative values, left and down; positive values, right and up. Dots indicate fixation (duration 100 ms) positions.

activities. This enlargement also led to an improved visual spatial orientation as well as object and scene identification (Zihl 2000).

Substitution of visual capacities by compensatory strategies

Oculomotor compensation of visual field defects

Compensation of visual field defects is mainly based on regaining of effective oculomotor gaze shifts to the visual environment into the region of visual field loss and on improving reading eye movements. Hemianopic patients may show short-term improvements in visual scanning (Zangemeister et al. 1995), but this adaptation is typically present in familiar surroundings only. The great majority of patients (about 80%) has difficulty in gaining a quick and complete overview, especially in unfamiliar surroundings. They have problems avoiding obstacles and with reading even several weeks after