Effects of prismatic adaptation on spatial gradients in unilateral neglect: A comparison of visual and auditory target detection with central attentional load

Prismatic adaptation is increasingly recognised as an effective procedure for rehabilitating symptoms of unilateral spatial neglect - producing relatively long-lasting improvements on a variety of spatial attention tasks. The mechanisms by which the aftereffects of adaptation change neglect patients’ performance on these tasks remain controversial. It is not clear, for example, whether adaptation directly influences the pathological ipsilesional attention bias that underlies neglect, or whether it simply changes exploratory motor behaviour. Here we used visual and auditory versions of a target detection task with a secondary task at fixation. Under these conditions, patients with neglect demonstrated a spatial gradient in their ability to orient to the brief, peripheral visual or auditory targets. Following prism adaptation, we found that overall performance on both the auditory and visual task improved, however, most patients in our sample did not show changes in their visual or auditory spatial gradient of attention, despite adequate aftereffects of adaptation and significant improvement in neglect on visual cancellation. Although there were individual cases that suggested prism-induced changes in visual target detection, and even reversal of the visual spatial gradient, such cases were not evident for the auditory modality. The findings indicate that spatial gradients in stimulus-driven attention may be less responsive to the effects of prism adaptation than neglect symptoms in voluntary orienting and exploratory behaviour. Individual factors such as lesion site and symptom severity may also determine the expression of prism effects on spatial neglect.     

Prismatic adaptation reduces biased temporal order judgements in spatial neglect

Visuomotor adaptation to rightward-deviating optical-wedge prisms reduces the clinical manifestations of spatial neglect after right hemisphere damage. We investigated whether this beneficial effect of prism adaptation is due to attenuation of the ipsilesional attentional bias that is common in spatial neglect. Five right hemisphere patients performed visual temporal order judgements before and after visuomotor adaptation to 15 degrees rightward-deviating prisms. The magnitude of patients' ipsilesional attentional bias on the temporal order judgement task was significantly reduced following adaptation. By contrast, the temporal order judgements of normal participants did not change following adaptation to either leftward- or rightward-deviating prisms. The findings suggest that prism adaptation helps to rebalance the distribution of spatial attention following right hemisphere damage.     

A kinematic analysis of distractor interference effects during visually guided action in spatial neglect.

Patients with left spatial neglect following right hemisphere damage may show anomalies in ipsilesional-limb movements directed to targets on their affected side, in addition to their characteristic perceptual deficits. In this study we examined the extent to which visually guided movements made by neglect patients are susceptible to interference from concurrent visual distractors on the contralesional or ipsilesional side of a designated target. Eleven right hemisphere patients with visual neglect, plus 11 matched healthy controls, performed a double-step movement task upon a digitizing tablet, using their ipsilesional hand to respond. On each double-step trial the first component of the movement was cued to a common central target, whereas the second component was cued unpredictably to a target on either the contralesional or ipsilesional side. On separate trials lateral targets either appeared alone or together with a concurrent distractor in an homologous location in the opposite hemispace. In addition to being significantly slower and more error prone than controls, neglect patients also exhibited a number of interference effects from ipsilesional distractors. They often failed to move to left targets in the presence of a right-sided distractor, or else they moved to the distractor itself rather than to a contralesional target. The initial accelerative phase of their movements to contralesional targets tended to be interrupted prematurely, and they spent significantly more time in the terminal guidance phase of movements to contralesional targets in the presence of an ipsilesional distractor. In contrast, contralesional distractors had little effect on patients' movements to ipsilesional targets. We conclude that right hemisphere damage induces a competitive bias that favors actions to ipsilesional targets. This bias affects multiple stages of processing within the visuomotor system, from initial programming through to the final stages of terminal guidance.     

A dissociation between visual and auditory hemi-inattention: Evidence from temporal order judgements

Patients with right hemisphere brain lesions often suffer from deficits in spatial attention that can be manifested in different sensory modalities. It has recently been claimed that a relationship (i.e., association) could exist between symptoms of hemi-inattention in different modalities, based on correlations between the results of visual and auditory clinical tests of neglect or extinction. However, it should be noted that the visual and auditory tasks varied greatly both in response type and level of sensitivity. Here, we have examined cross-modal associations in spatial attention deficits using a temporal order judgment task (TOJ) in which patients were required to identify which of two visual or auditory objects had appeared first. When compared to age and education matched control participants, the patients needed, on average, the contralesional stimulus to lead the ipsilesional stimulus to achieve the point of subjective simultaneity (PSS). No association between the degree of visual and auditory hemi-inattention was observed amongst the patients, suggesting that there is a certain degree of independence between the mechanisms subserving spatial attention across sensory modalities.     

Grey scales uncover similar attentional effects in homonymous hemianopia and visual hemi-neglect

Multi-component models of visual hemi-neglect have postulated that visual hemi-neglect is characterised by various attentional deficits. A grey scales task has been developed to quantify the early, automatic, (perhaps obligatory) ipsilesional orienting of visual attention, frequently assumed as the first of these attentional deficits. Explanations for this attentional imbalance are up until now mainly formulated in terms of right hemisphere activation. This lateral attentional bias has also been demonstrated in controls, in whom it is expressed as a leftward perceptual asymmetry. We reproduced previous literature findings on a grey scales task, considering controls and neglect patients. Three patients with neglect showed an extreme ipsilesional lateral bias. This bias did not change during or after cognitive rehabilitation. Additionally, we presented this grey scale task to 32 patients with left- and right-sided homonymous hemianopia (HP). HP is the loss of sight in one visual hemi-field. The HH patients had no clinical signs of impaired lateralised attention. Results revealed that HH patients showed a similar ipsilesional bias, albeit to a lesser degree than in neglect. Left-sided HH patients presented a quantitatively similar, but qualitatively opposite bias than the right-sided HH patients. We suggest that sensory effects can be an alternative source of attentional imbalance, which can interact with the previously proposed (right) hemispheric effects. This suggests that the perceptual asymmetry in the grey scales task is not necessarily an indicator of impaired right hemisphere attention. It rather suggests a pattern of functional cerebral asymmetry, which can also be caused by asymmetric sensory input.     

Selective deficit of auditory localisation in patients with visuospatial neglect.

Possible auditory deficits in neglect were examined by comparing the performance of four right brain-damaged (RBD) patients with left visuospatial neglect, versus four RBD patients without neglect, in three auditory tasks. The first task required speeded discrimination of sound elevation, by moving a central lever up or down according to the vertical position of a peripheral target sound, regardless of its side. The other two auditory tasks were non-spatial, requiring either speeded pitch discrimination (moving the central lever up for high pitch, down for low pitch) or speeded target detection. Neglect patients' performance was impaired with respect to RBD controls only when the auditory task required spatial coding of the target sound (the up/down spatial discrimination). This demonstrates a selective deficit of auditory space perception in neglect patients. This auditory spatial deficit was more pronounced for left than right sounds. Since auditory space perception was impaired in the vertical dimension, the observed deficit cannot be attributed to a systematic rightward shift in sound localisation. Instead, the results suggest increased spatial uncertainty in sound localisation by neglect patients, particularly for auditory targets on the contralesional side. These findings are related to multimodal coding of space in the parietal cortex, which was damaged in the neglect patients, but not in the RBD controls.     

Auditory deficits in visuospatial neglect patients

Since the pioneering experimental work of Bisiach et al. (1984) on deficits in sound localisation associated with unilateral brain lesions and visual neglect, a number of systematic investigations have examined auditory processing in visuospatial neglect patients. Evidence from a variety of experimental paradigms has revealed some auditory deficits in detection and identification tasks, during bilateral stimulation; plus localisation deficits for single sounds. These deficits emerge predominantly for contra-lesional sounds, although some auditory disturbances applying to both contra- and ipsilesional sounds have also been documented. Here we review evidence suggesting that some of these auditory deficits arise in relatively high-level stages of spatial processing. In addition, we present new analyses showing that auditory deficits in identification and localisation tasks often correlate with clinical measures of visual neglect, across a variety of different studies and tasks. This empirical relation suggests that a disturbance of multisensory spatial processing may often account for the joint auditory and visual spatial deficits in neglect patients, although rarer dissociations between the modalities should also be considered.     

Impaired spatial working memory: one component of the visual neglect syndrome?

Both impaired spatial working memory (SWM) and unilateral neglect may follow damage to the right parietal lobe. We propose that impaired SWM can exacerbate visual neglect, due to failures in remembering locations that have already been searched. When combined with an attentional bias to the ipsilesional right side, such a SWM impairment should induce recursive search of ipsilesional locations. Here we studied a left neglect patient with a right temporoparietal haemorrhage. On a nonlateralised, purely vertical SWM task, he was impaired in retaining spatial locations.

In a visual search task, his eye position was monitored while his spatial memory was probed. He recursively searched through right stimuli, re-fixating previously inspected items, and critically treated them as if they were new discoveries, consistent with the SWM deficit. When his recovery was tracked over several months, his SWM deficit and left neglect showed concurrent improvements. We argue that impaired SWM may be one important component of the visual neglect syndrome.     

Gaze direction modulates auditory spatial deficits in stroke patients with neglect

We investigated the effects of eye position on auditory spatial deficits in four patients with left neglect and right-hemisphere damage, using three blocked gaze directions (35 degrees to the right, central, or 35 degrees to the left), while preventing any head-movement to ensure that initial auditory inputs remained constant regardless of eye-in-orbit position. The auditory task required speeded discrimination of sound elevation, with patients moving a central lever up or down according to the vertical position of a peripheral target sound, regardless of its side (left or right). Replicating previous auditory research, the patients' vertical discrimination performance was worse for auditory targets on the contralesional (left) versus the ipsilesional side, indicating neglect-related auditory deficits on this task. Critically, while this worse performance for left than right auditory targets was present (for both reaction times and errors) when gaze was directed centrally or rightwards, it was considerably reduced when gaze was directed leftwards. These results demonstrate that lateral gaze-direction can modulate neglect-related auditory spatial deficits, even though eye-position did not alter the initial auditory inputs. This outcome may relate to audio-visual links in spatial orienting and potentially some retinocentric influences on perceived sound location, although the latter alone could not explain all our results. Such findings might involve multisensory brain structures in which responses to sounds are modulated by eye-in-orbit position.     

Deficit of auditory space perception in patients with visuospatial neglect

There have been many studies of visuospatial neglect, but fewer studies of neglect in relation with other sensory modalities. In the present study we investigate the performance of six right brain damaged (RBD) patients with left visual neglect and six RBD patients without neglect in an auditory spatial task. Previous work on sound localisation in neglect patients adopted measure of sound localisation based on directional motor responses (e.g., pointing to sounds) or judgement of sound position with respect to the body midline (auditory midline task). However, these measures might be influenced by non-auditory biases related with motor and egocentric components. Here we adopted a perceptual measure of sound localisation, consisting in a verbal judgement of the relative position (same or different) of two sequentially presented sounds. This task was performed in a visual and in a blindfolded condition. The results revealed that sound localisation performance of visuospatial neglect patients was severely impaired with respect to that of RBD controls, especially when sounds originated in contralesional hemispace. In such condition, neglect patients were always unable to discriminate the relative position of the two sounds. No difference in performance emerged as a function of the visual condition in either group. These results demonstrate a perceptual deficit of sound localisation in patients with visuospatial neglect, suggesting that the spatial deficits of these patients can arise multimodally for the same portion of external space.     

Ipsilesional versus contralesional neglect depends on attentional demands

Right hemisphere injuries often produce contralesional hemispatial neglect (CN). In contrast to CN, some patients with right hemisphere damage can also show so-called ipsilesional neglect (IN). Previous reports found that patients tend to show IN on line bisection tasks but CN on other tasks such as target cancellation. To learn why these two tasks induce different spatial biases in patients with right hemisphere injury, conventional (i.e. solid) line bisection was compared with two novel bisection tasks consisting of horizontally aligned strings of characters. The subjects' task was to mark a target character that was at or closest to the true midpoint of the simulated line. Four of the 5 patients showed a dissociation whereby IN occurred for solid lines while CN was observed on character lines. The two patients assessed with an antisaccade paradigm showed a "visual grasp" for leftward stimuli. The present results suggest that neglect on line bisection may reflect two opposing forces, an approach behavior or "visual grasp" toward left hemispace and an attentional bias toward right hemispace.     

Prism adaptation and spatial attention: a study of visual search in normals and patients with unilateral neglect

Visuomotor adaptation to a prism-induced lateral displacement of the visual field induces mild perceptual biases in healthy individuals and improves symptoms of unilateral neglect. The present study employed a speeded visual search task to test the hypothesis that prism adaptation induces an adaptive redistribution of selective spatial attention. In Experiment 1, 32 neurologically healthy, right-handed participants were adapted to a 15° prism–induced lateral (left or right) displacement of the visual field. Spatial attention was measured by search time and error-rate in unique-feature (“preattentive”) and feature-absent (“serial”) visual search tasks, before and after prism adaptation. The single target appeared at different locations within arrays of 12, 24 or 48 items. Contrary to the attentional hypothesis, the pattern of search performance across the display remained unchanged following prism adaptation. In Experiment 2, we tested four patients with unilateral right hemisphere damage on the visual search tasks, before and after adaptation to 15° rightward-displacing prisms. All four patients showed a pathological gradient of spatial attention toward the ipsilesional side prior to adaptation. Consistent with the results from Experiment 1, the gradient in search performance shown by the patients did not change following prism adaptation. Taken together, these findings suggest that the perceptual aftereffects in normals and amelioration of unilateral neglect following prism adaptation are not mediated by an adaptive redistribution of spatial attention.     

Visual localization of sounds

Circumscribed hemispheric lesions in the right hemisphere have been shown to impair auditory spatial functions. Due to a strong crossmodal links that exist between vision and audition, in the present study, we have hypothesized that multisensory integration can play a specific role in recovery from spatial representational deficits. To this aim, a patient with severe auditory localization defect was asked to indicate verbally the spatial position where the sound was presented. The auditory targets were presented at different spatial locations, at 8 degrees, 24 degrees, 40 degrees, 56 degrees to either sides of the central fixation point. The task was performed either in a unimodal condition (i.e., only sounds were presented) or in crossmodal conditions (i.e., a visual stimulus was presented simultaneously to the auditory target). In the crossmodal conditions, the visual cue was presented either at the same spatial position as the sound or at 16 degrees or 32 degrees, nasal or temporal, of spatial disparity from the auditory target. The results showed that a visual stimulus strongly improves the patient's ability to localize the sounds, but only when it was presented in the same spatial position of the auditory target.     

Ipsilesional Bias and Processing Speed are Important Predictors of Functional Dependency in the Neglect Phenomenon After a Right Hemisphere Stroke

Visuospatial neglect (VSN) predicts unfavorable functional outcome in stroke patients. This study examined the relative importance of different core symptoms of VSN as predictors of functional dependency. A consecutive series of 105 right hemisphere stroke patients were tested early after stroke on three basic symptoms of VSN (omissions, asymmetry of omissions and ipsilesional bias of attention) and on two symptoms related to VSN (processing speed and repetitive target detections in visual search). Neurological deficits were also assessed. Functional outcome was measured 3 months and 2 years after stroke with the modified Rankin Scale. Univariate analyses revealed significant relationships with functional outcome for both core and related symptoms of VSN and for neurological deficits. Area under the curve statistics and stepwise logistic regressions showed that the most important predictors assessed early after stroke were presence of ipsilesional bias for dependency at 3 months and visual processing speed for dependency at 2 years after stroke. These results show that valuable prognostic information regarding dependency after right hemisphere stroke can be obtained by assessing fundamental sub-components of VSN early after stroke. The development of standardized clinical methods for investigation of sub-components, such as a right capture of attention and processing speed, is essential.     

Visual search patterns in neglect: Comparison of peripersonal and extrapersonal space

Previous studies of visual search patterns in visuospatial neglect have analyzed shifts of attention during search tasks using eye tracking technology and verbal reports. The purpose of the present study was to replicate and extend upon reported parameters of visual scanning patterns of neglect patients in peripersonal space (within arms reach) and to examine whether similar patterns of visual search are also apparent in extrapersonal space (beyond arms reach). Using a simple verbal visual search and target detection paradigm right-hemisphere stroke participants, with and without neglect, and healthy older volunteers named targets on scanning sheets placed in peripersonal and extrapersonal space. The healthy controls and right-hemisphere stroke group without neglect showed similar ‘reading’ type strategies, while the neglect group displayed an unsystematic search pattern, during search in both peripersonal and extrapersonal space. Group comparisons of search parameters support the presence of multiple cognitive deficits affecting the complex visual search patterns of neglect patients, including a rightward attentional bias, a reduced spatial scale of attention (local processing bias), and a deficit of working memory affecting both near and far space search. Ventral visual stream damage and neglect, however, were related to slower target report rate and more misidentification errors in extrapersonal space. The ease of administration of this verbal target detection task in both peripersonal and extrapersonal space, and the relationship of the measures produced to theorized attentional and executive deficits in neglect, provide impetus for further research on the severity and independence of individual scanning deficits in neglect.     

Line bisection under an attentional gradient induced by simulated neglect in healthy subjects

Whether an attentional gradient favouring the ipsilesional side is responsible for the line bisection errors in visual neglect is uncertain. We explored this by using a conjunction-search task on the right side of a computer screen to bias attention while healthy subjects performed line bisection. The first experiment used a probe detection task to confirm that the conjunction-search task created a rightward attentional gradient, as manifest in response times, detection rates, and fixation patterns. In the second experiment subjects performed line bisection with or without a simultaneous conjunction-search task. Fixation patterns in the latter condition were biased rightwards as in visual neglect, and bisection also showed a rightward bias, though modest. A third experiment using the probe detection task again showed that the attentional gradient induced by the conjunction-search task was reduced when subjects also performed line bisection, perhaps explaining the modest effects on bisection bias. Finally, an experiment with briefly viewed pre-bisected lines produced similar results, showing that the small size of the bisection bias was not due to an unlimited view allowing deployment of attentional resources to counteract the conjunction-search task's attentional gradient. These results show that an attentional gradient induced in healthy subjects can produce visual neglect-like visual scanning and a rightward shift of perceived line midpoint, but the modest size of this shift points to limitations of this physiological model in simulating the pathologic effects of visual neglect.     

Impact of dynamic bottom-up features and top-down control on the visual exploration of moving real-world scenes in hemispatial neglect

Patients with hemispatial neglect are severely impaired in orienting their attention to contralesional hemispace. Although motion is one of the strongest attentional cues in humans, it is still unknown how neglect patients visually explore their moving real-world environment. We therefore recorded eye movements at bedside in 19 patients with hemispatial neglect following acute right hemisphere stroke, 14 right-brain damaged patients without neglect and 21 healthy control subjects. Videos of naturalistic real-world scenes were presented first in a free viewing condition together with static images, and subsequently in a visual search condition. We analyzed number and amplitude of saccades, fixation durations and horizontal fixation distributions. Novel computational tools allowed us to assess the impact of different scene features (static and dynamic contrast, colour, brightness) on patients' gaze. Independent of the different stimulus conditions, neglect patients showed decreased numbers of fixations in contralesional hemispace (ipsilesional fixation bias) and increased fixation durations in ipsilesional hemispace (disengagement deficit). However, in videos left-hemifield fixations of neglect patients landed on regions with particularly high dynamic contrast. Furthermore, dynamic scenes with few salient objects led to a significant reduction of the pathological ipsilesional fixation bias. In visual search, moving targets in the neglected hemifield were more frequently detected than stationary ones. The top-down influence (search instruction) could neither reduce the ipsilesional fixation bias nor the impact of bottom-up features. Our results provide evidence for a strong impact of dynamic bottom-up features on neglect patients' scanning behaviour. They support the neglect model of an attentional priority map in the brain being imbalanced towards ipsilesional hemispace, which can be counterbalanced by strong contralateral motion cues. Taking into account the lack of top-down control in neglect patients, bottom-up stimulation with moving real-world stimuli may be a promising candidate for future neglect rehabilitation schemes.     

Cross-modal interactions in time and space: auditory influence on visual attention in hemispatial neglect

Recent studies indicate that auditory tone presentation and auditory alerting can temporarily ameliorate visuospatial attention deficits in patients with unilateral neglect [Frassinetti, F., Pavani, F., & Ladavas, E. Acoustical vision of neglected stimuli: Interaction among spatially converging audiovisual inputs in neglect patients. Journal of Cognitive Neuroscience, 14, 62-69, 2002; Robertson, I. H., Mattingley, J. B., Rorden, C., & Driver, J. Phasic alerting of neglect patients overcomes their spatial deficit in visual awareness. Nature, 395, 169-172, 1998]. The current study investigated proposed mechanisms of cross-modal interaction to determine conditions in which auditory stimulation affects spatial and nonspatially lateralized attention deficits in a patient with hemispatial neglect. In Experiment 1, a target was presented among related distracters (conjunction search) while a tone was presented either bilaterally or in a congruent or incongruent spatial location with respect to the visual target. Whereas the results suggest a benefit of both general alerting and cross-modal spatial integration on visual search efficiency, the most significant improvement occurred when the target and tone were both presented in contralesional space. In Experiment 2, the effect of auditory alerting on selective attention was examined in a rapid serial visual search procedure with visual targets embedded in a stream of distracters presented at central fixation. When two targets were presented without an alerting tone, the patient missed the second target for up to 1000 msec after the first target appeared (a finding known as the "attentional blink" [AB] and, on average, about 400-500 msec in normals). An alerting tone presented at a fixed temporal location significantly reduced the AB in a tone-duration-dependent manner. Experiment 3 examined the effect of cross-modal space on selective attention in an AB paradigm in which T2 occurred randomly to the left or right of T1 with a spatially congruent or incongruent tone. Discrimination of T2 in contralesional space significantly improved when the tone was presented in the same location, and was impaired when the tone was presented on the ipsilesional side. The findings are discussed as they relate to cross-modal interactions and their influence on spatial and nonspatially lateralized attention deficits in neglect.     

Disturbed sound lateralization in patients with spatial neglect

Previous studies on auditory space perception in patients with neglect have investigated localization of free-field-sound stimuli or lateralization of dichotic stimuli that are perceived intracranially. Since those studies in part revealed contradictory results, reporting either systematic errors to the left or systematic errors to the right, we reassessed the ability of auditory lateralization in patients with right hemispheric lesions with and without neglect. Unexpectedly, about half of the patients with neglect showed erratic judgments on sound position, that is, they were completely unable to lateralize sounds. The remaining neglect patients only showed a small deviation of the auditory median plane to the left side, indicating that they perceived the sounds as slightly shifted to the right side. The comparison between both groups revealed higher severity of neglect in the group of neglect patients who were unable to perform the task, suggesting that the inability of sound lateralization was associated with the strength of clinical neglect. However, we also observed 1 out of 9 patients with left brain damage who was not able to lateralize spatial sounds. This patient did not show any symptoms of spatial neglect. Thus, it may be that a spatial auditory deficit, such as that observed here in right-brain-damaged patients, only co-occurs with spatial neglect if the right superior temporal cortex is lesioned.     

Competition between simultaneous stimuli modulated by location probability in hemispatial neglect

Many aspects of spatial neglect can be explained as arising from competition for attentional selection, with salient ipsilesional stimuli emerging as the winner more often than contralesional stimuli. The outcome of the competition, however, can be affected both by bottom-up perceptual factors such as the gestalt properties of the display and by top-down factors such as expectancy or stimulus blocking. This study examines whether the competition for attentional selection can be modulated by manipulating the probability of the target's location in hemispatial neglect. Five patients with left-sided hemispatial neglect and a group of control participants performed a visual target discrimination task. In equal probability blocks, the target appeared randomly in any of six possible horizontal locations (three left, three right) whereas in biased blocks, the target appeared in the mid-location on the left on 50% of the trials and in each of the other locations on 10% of the trials. The target appeared either alone or was accompanied by a distractor on the opposite side. The results showed that the spatial bias facilitated detection of all left-sided targets in the neglect group, but was more spatially specific in the control group. Furthermore, while distractors on either side interfered with target processing in both groups, the patterns differed across the visual field. Finally, the magnitude of facilitation due to the bias was greatest in the condition with the most inhibition, i.e. a left-sided target accompanied by a right-sided distractor in the neglect group. These data underscore the competitive push-pull relationship between different bottom-up and top-down attentional factors, particularly within neglect patients, in whom a strong ipsilesional attentional bias already exists.