Introduction
Homonymous hemianopia (HH), the loss of vision in one half of the visual field, results from unilateral lesions of the geniculostriate pathway. Although a degree of spontaneous recovery may occur in some patients with HH [
1‐
4] it is rarely sufficient to remove the disabling consequences of visual field loss—difficulties in reading, driving and visual exploration, and deficits of visuo-spatial orientation [
5,
6]. Although a small minority of patients with hemianopia appear to retain sensitivity to briefly flashed or moving stimuli within their blind field [
7], this residual vision appears inaccessible to conscious perception and action.
Rehabilitation of patients with HH, once thought an untreatable condition, has recently become a matter of intense debate (see [
8] for a review). Several groups have claimed restitution of visual function and consequent visual field enlargement by repeated visual stimulation, usually at the border of the scotoma [
9‐
15] and changes in cortical representation in the pre-striate cortex as a result of training have also been reported [
16]. Other studies have found no effect of training on visual field enlargement [
17‐
20]. However, rigorous control of fixation during training eliminates significant visual field enlargement [
20], an observation which has led to controversy over the very existence of visual field enlargement [
14,
21‐
23].
An alternative rehabilitation technique is visual search training, which aims to adapt patients’ scanning strategies to most effectively compensate for their visual field loss. In some cases, HH disrupts normal scanning patterns with patients exhibiting disorganised scanpaths with high rates of refixation and inaccurate saccades [
24] and it has been proposed that the loss of re-entrant pathways from higher visual areas to the damaged striate cortex may result in uncertainty about spatial locations across saccades [
3]. Some patients make a series of small saccades, with long latencies into their blind field [
25‐
27]. In light of these scanpath abnormalities, patients are often trained to make systematic horizontal or vertical scanning saccades into their blind field (oculomotor training) [
5,
24,
27‐
29]. Training usually leads to an enlargement of the region in which subjects can successfully locate a target with eye movements (the visual search field, VSF) and a reduction in response times [
5,
29‐
31]. Importantly, training also leads to improvements in activities of daily living (ADLs), assessed both empirically as well as with subjective questionnaires [
24,
28‐
30]. However several questions concerning visual search training remain unresolved. Firstly, most patients, even without training, learn to compensate for their field loss by making more fixations and spending a greater proportion of viewing time in their “blind” half-field [
24,
32‐
34] and there is evidence that this compensatory strategy evolves over time [
26]. Does specific training therefore simply reinforce these naturally occurring strategies or does it, in fact, further alter the efficacy of search eye movements? Secondly, as repeated visual search practise leads to perceptual learning can the reductions in response times associated with visual search training be explained by neuronal changes in response to the learnt stimulus features, rather than changes in eye movement strategies? Several recent studies have attempted to answer these questions by evaluating oculomotor behaviour in patients with HH following oculomotor training [
35,
36] or training on extended visual search containing multiple targets [
37]. By contrast, Pambakian et al. [
30] trained 29 patients with homonymous visual field defects to perform visual search without prescribing any particular oculomotor strategy to patients, reasoning that repeated visual search practise with search durations of 3 s or less would allow patients to develop their own adaptive scanpaths [
38]. As a group, patients in this study evinced larger VSF after training, together with a significant mean reduction of response times. The focus of the current paper is to characterise the changes in oculomotor scanning that resulted from training.
Discussion
Visual search training in a group of 29 patients with homonymous hemianopia led to a number of
training-specific changes in saccadic behaviour accompanied by significant reduction in the mean search times required to locate a single target amongst distractors [
30]. After visual search training patients made a higher proportion of fixations into the hemispace containing the target; patients were quicker to switch into the hemifield containing the target
if the initial saccade had been made into the opposite hemifield; patients made fewer transitions from one hemifield to another before locating the target; patients made a larger initial saccade, although the direction of the initial saccade did not change, and there was a very small but significant increase in the number of saccades made in the direction of the target after training. In addition, patients required fewer saccades to locate the target after training, reflecting increased search efficiency and the area within which targets could be fixated in the blind field also increased. These changes were specific to the period of training, i.e. there was no spontaneous change or improvement between visits 1 and 2 (the visits prior to the training phase). Moreover all the changes seen after training at visit 3 were maintained at visit 4 (a month after the training had been completed).
Previous visual search rehabilitation programs designed to treat deficits in visual exploration have primarily aimed at improving disorders of visuo-spatial disorientation apparent in some patients with HH. Thus these training programs require patients to search for a number of targets over an extended time period and have explicitly instructed patients to make large initial saccades into the hemianopic hemifield, and to search in a rigid systematic manner [
5,
24,
28,
31,
32,
35,
36] or through extended visual search training [
37]. By contrast we trained [
30] subjects to search for a single target for 3 s or less, and did not suggest any particular oculomotor behaviour. Schuett et al. [
34] have shown that healthy volunteers with simulated hemianopias adopt spontaneous oculomotor compensatory strategies following a very short single period of visual search training [
34]. Although healthy volunteers with simulated hemianopias cannot be directly compared to patients with brain damage, our results demonstrate that patients, left to themselves, also adopt a subtle and effective visual search strategy, in our case, after a prolonged period of training.
The efficacy of visual search training in patients with HH depends critically on whether improvements in visual search generalise from the stimuli used in training to everyday visual search tasks. While one recent study found that visual search training resulted in compensatory oculomotor scanning in a picture viewing task [
37], a study of simulated HH in healthy volunteers found no evidence of transfer between tasks [
38]. Another recent study of oculomotor training in patients with HH resulted in adaptive changes during visual search, only if the oculomotor training involved audio-visual, rather than visual stimuli [
35] in contrast to our study, where visual search training without auditory cues was sufficient to produce compensatory eye movements.
A related question is whether the changes in oculomotor scanning reflect
genuine changes in oculomotor strategy or are consequent upon neuronal tuning or neuronal plasticity in the visual cortex. For example, visual functions such as stereoacuity, orientation and motion detection, segmentation of textures and hyperacuity improve after prolonged practise [
42,
43]. Because learning for these visual features tends to be very specific, often confined to the trained visual field location, or trained orientation or motion, with little transfer to the untrained eye, low-level changes in neuronal tuning, e.g. in V1, have been implicated. In contrast, perceptual learning in visual search has been shown to transfer over retinal locations, and from the trained to the untrained eye. Some studies have shown no transfer of learning to novel visual search tasks [
42,
43], whereas others studies have found far less specificity [
44‐
47]. These latter authors suggest that training in visual search initially involves neuronal changes in regions high in the visual brain—for example, practise in orientation discrimination leads to narrower orientation tuning curves in macaque V4—and involve changes in the deployment of visuo-spatial attention. Some of the oculomotor behaviour documented here may result from perceptual learning. For example fixation durations in the intact hemispace are shorter after training. One interpretation of this finding is that visual search practise results in perceptual learning, facilitating target detection prior to—and during—fixation on target (hence lower fixation durations). Fixation durations for targets in hemianopic space remain unchanged as low-level perceptual learning cannot occur in the damaged striate cortex. The effect of this postulated perceptual learning disappears once visual search training has ceased.
Other findings within our study suggest the existence of
cognitive changes in strategy. We found that the mean saccadic amplitude did
not increase after training, as would be expected if neuronal changes resulted in improved tuning specific to the search stimuli. Patients also learnt to saccade more quickly into the hemianopic hemifield when the target was also in the hemianopic field—even though their HH would prevent them detecting these targets. The visual lobe size—the area within the blind field within which patients could saccade successfully to the target—also increased after training. This may appear surprising as visual field perimetry demonstrated no increase in visual fields after training [
30]. However the increasing lobe size may simply reflect more efficient placement of the eyes after training, allowing patients to saccade to the probable location of the target. The notion that visual search improvements are strategically based is also supported by the finding [
30] that patients demonstrated significant improvements, on the order of a 25% reduction in response times, for tasks of daily living involving novel visual search stimuli.
The scanning behaviour of patients during search demonstrates a close interplay between bottom-up visual influences and top-down strategic ones. So, for example, the proportion of fixations made in hemianopic hemispace and the proportion of initial saccades made into the hemianopic hemifield were significantly higher than 50%
only when the target was in hemianopic hemispace. This contrasts with hemianopic scanning for natural scenes [
26], where we found that patients with long-standing hemianopias, indeed made more fixations and spent a greater proportion of their viewing time in hemianopic hemispace. In that study hemifield differences were accentuated when images were filtered to remove much of the semantic and visual content of the scene, and the authors suggested that top-down cognitive adaptive strategies play an increasing role in directing eye movements in the absence of semantic/visual information. In a carefully controlled, randomized study Roth et al. [
37] found that patients altered their eye movement patterns following visual search therapy, placing a higher proportion of their fixations in the blind half field during free scene inspection, even if the salient object within the scene was located on the seeing side. It thus appears that strategic guidance of eye movements is task specific; in the current study, where subjects were required to search for a target equally likely to appear in either hemifield, patients did not automatically bias their eye movements to hemianopic hemispace—thereby automatically rendering eccentric ipsilesional targets more difficult to detect—and, instead, adopted a more advantageous strategy of more rapid switching of hemifields as a result of training. Homonymous visual field defects are a common consequence of stroke; 30% of all patients with stroke [
48] and 70% of patients with stroke involving the posterior cerebral artery have such field defects [
49]. Homonymous visual field defects are associated with a poor prognosis for recovery [
50‐
53], particularly when combined with visual hemispatial neglect [
54‐
57] and yet there are still no established rehabilitation programs for such patients. The efficacy visual restoration therapy is still subject to consideration [
20‐
23] and requires 6 months of training. Visual restoration studies either involve repeated stimulation at the borders of a scotoma or deep within the blind field with the aim of stimulating extra-striate cortex. Both methods can generate unwanted eye movements [
11,
18,
20‐
22]. In fact, where stimuli are repeatedly presented in the blind field for >0.5 s durations during training, part of the “restitution” may actually result from patients learning efficient oculomotor strategies, as patients did here, and that allow them to localise the target within the presentation time [
16,
58,
59].
Here we have shown that visual search training for short stimulus durations, results in effective adaptive oculomotor strategies. The results of this paper complement an earlier paper [
30] in which we demonstrated the transfer of visual search training to activities of daily living and significant subjective improvements in the same patients. The visual search training method described here is short (1 month duration), inexpensive, and can be conducted by patients in their own homes without the intervention of a therapist. Importantly, however, our present study
cannot disentangle the effects of training from the potential role of spontaneous recovery. A future study with a
hemianopic control group undergoing testing in four sessions but no training would be required to rule out the role of spontaneous recovery. Spontaneous oculomotor adaptation in patients with homonymous hemianopia is very well documented [
25,
27,
33,
57] although hemianopic patients with additional damage to occipito-parietal cortex or posterior thalamus appear less likely to spontaneously adopt compensatory oculomotor strategies [
24]. An earlier small cross-sectional study of hemanopic patients suggests a relatively long time-course for spontaneous recovery which takes 6 months to develop and may continue to evolve for over a year [
26]. Although the majority (72%) of our patients were recruited >1 year after onset, it is possible that spontaneous adaptation could coincide with the critical month of training between sessions 2 and 3, but not occur during sessions 1 and 2. In response to clinical need, however, a DVD of the entire visual search program is available at
http://vision.metope.org. And in support of our findings, a recent study where patients were randomly assigned to a visual search training or visual restitution training group found that only patients in the former group demonstrated oculomotor changes and subjective benefits in activities of daily living [
37].