Revisiting unilateral neglect

Unilateral neglect, a neurological disorder in which patients fail to detect or respond to contralesional stimuli, has long been considered a failure of attentional orienting mechanisms. This review provides a selective overview of the prominent biases in spatial orienting and exploratory motor behaviour observed in these patients before considering the impact of other factors on the presentation of the disorder and how those factors might inform current neurological models of neglect. In the latter part of the review, we intend to suggest that neglect is likely to be a combination of distinct but interacting impairments including biases in attentional orienting, exploratory motor behaviours and a deficit of spatial working memory. That is, we suggest that the cardinal symptom of neglect - a loss of awareness for contralesional stimuli and events - arises as a result of a combination of these impairments rather than being associated solely with the more dramatic and immediately evident biases in spatial attention.     

Hypermnesia in unilateral neglect

Thirteen right brain-damaged patients who were found to neglect pictures presented on the left of a display were presented the same stimuli, intermixed with foils, in a yes-no recognition test. Fifty per cent of patients claimed to have already seen one or more of the previously neglected pictures. This demonstrates that visual information that fails to access consciousness in neglect patients does retain the ability to surface as explicit memory at a later stage.     

Searching with unilateral neglect

We address two longstanding conflicts in the visual search and unilateral neglect literature by studying feature and conjunction search performance of neglect patients using laterally presented search arrays. The first issue relates to whether feature search is performed independently of attention, or rather requires "spread attention." If feature search is "preattentive," it should survive neglect. However, we find neglect effects for both feature and conjunction search, suggesting that feature search, too, has an attentional requirement. The second controversy refers to the space- or object-based nature of neglect following unilateral right-hemisphere parietal lobe damage. If neglect were a purely spatial phenomenon, then we would expect no detriment in performance in the right (nonneglect) field, and diminished performance for the whole left (neglect) field. On the other hand, if neglect were purely object-based, we would expect diminished performance on the left side of the search array, irrespective of its location in the visual field. We now demonstrate a combination of strong object-based and space-based neglect effects for conjunction search with laterally placed element arrays, suggesting that these two mechanisms work in tandem.     

Recovery from unilateral neglect

Spontaneous recovery of function occurs in the syndrome of hemisensory neglect in monkeys. We produced this syndrome in 13 macaques by unilateral operative resection of the frontal polysensory association cortex. Using standardized behavioral measures, we documented severe acute neglect and followed the course of its improvement. Using the 2-deoxy[¹⁴C]glucose autoradiographic method, we studied animals in the acute phase of neglect and found decrements in local glucose utilization in subcortical structures, but not in cortical regions with known frontal connections. After spontaneous behavioral recovery, mild local glucose utilization decrements remained, but only in nucleus medialis dorsalis of the thalamus. The findings suggest that acute behavioral symptoms are based on widespread depression of neuronal activity in uninjured structures with synaptic relations to damaged cortex, and that return of neuronal activity in those structures is accompanied by restitution of behavioral function.     

Caloric stimulation and unilateral visual neglect

We studied performance on tests of visual neglect and left lateral gaze after caloric stimulation in 18 patients with left-sided visual neglect after strokes. Except for one patient with absent vestibulo-ocular responses, all improved during caloric stimulation on the left by cold (LC) or on the right by warm water (RW). Improvement seemed to depend on the facilitation of left lateral gaze and on past-pointing to the left. During LC and RW caloric stimulation, patients worked from left to right instead of their usual right to left. Caloric stimulation may be of use in training patients with hemispatial neglect to orient toward the affected hemispatial field.     

Context and crossover in unilateral neglect

Patients with left-neglect bisect horizontal lines to the right of true center. Their bisection bias is affected by line length, so that longer lines are bisected further to the right. Patients often crossover and bisect very short lines to the left of true center. We tested the hypothesis that the context in which lines are apprehended accounts for the crossover phenomenon. We replicated previous findings that a line is bisected further leftward when it is preceded by a longer line and further rightward when it is preceded by a shorter line. These contextual effects occur with relatively short and relatively long target lines. Bisection patterns in two different series of lines, one ranging from 10 to 150 mm, and the other from 110 to 250 mm, were investigated. If crossover bisections were simply due to contextual effects then left-sided errors would be observed on bisections of the shorter lines of both series. Our findings did not support this hypothesis. Crossover bisections occurred only with objectively short lines, those shorter than 40 mm. Even though we found significant contextual effects on line bisection biases, these effects per se do not account for the crossover phenomenon. Rather, our data suggest that the absolute length of the line is associated specifically with the crossover phenomenon.     

Mirror images and unilateral spatial neglect

Responding correctly to a mirror image requires the creation of a rather peculiar form of dual representation. Mirror agnosia and mirror ataxia, i.e. a deficit in reaching an object reflected in a mirror, have been reported to be associated with parietal lobe lesions. This prospective study was conducted to investigate the capacity of subjects with neglect to identify the mirror image nature of visual information. Four consecutive brain-damaged patients with neglect, selected on the basis of specific criteria, and four control subjects performed grasping and object displacement tests under two response conditions (normal mirror and inverted mirror). Video recordings of the tests were analyzed to assess performance using the following criteria: (i) direction of the arm movement during the initial phase of movement, (ii) number of corrections of the hand position before grasping. The control subjects successfully grasped the objects in both experimental conditions. The patients (1) neglected the contralesional space, grasping objects correctly in the ipsilesional space (normal mirror condition) and (2) neglected the ipsilesional space, grasping correctly objects in the contralesional space (inverted mirror). Controls used real object-centered correction clues to modify the position and direction of their hand movement. The patients only produced horizontal displacements of the upper limb in the ‘healthy’ and neglected space. These results suggest that patients with neglect do not use the same clues and do not modify their procedures as they cannot recalibrate their spatial representations. These differences concerned non-mirror-image clues and directional and positional as well as attentional vectors. Theoretical and rehabilitative implications are discussed.     

Dopaminergic stimulation in unilateral neglect

OBJECTIVE—To explorethe hypothesis that dopaminergic circuits play a part in the premotorcomponents of the unilateral neglect syndrome, the effects of acutedopaminergic stimulation in patients with neglect were studied.
METHODS—Two tasks wereevaluated before and after subcutaneous administration of apomorphineand placebo: a circle crossing test and a test of target exploration (amodified version of the bell test), performed both in perceptual(counting) and in perceptual-motor (pointing) conditions.
SUBJECTS—Four patientswith left neglect.
RESULTS—Afterdopaminergic stimulation, a significant improvement was found comparedwith placebo administration and baseline evaluation, in the performanceof the two tests. Three of the patients had a more marked improvementin the perceptual-motor condition (pointing) of the task than theperceptual condition (counting).
CONCLUSIONS—Thefindings suggest that dopaminergic neuronal networks may mediate, indifferent ways, both perceptive and premotor components of theunilateral neglect syndrome.

     

Is there a correlation between motor neglect and unilateral sensory neglect

Similarities between motor neglect and unilateral sensorial neglect are so striking that their mechanisms are likely to be almost the same. As the attentional interpretation is no longer possible for motor neglect, and the intentional interpretation may be dismissed in man because of the loss of automatic movements, the psychological interpretation must be abandoned. A purely physiological hypothesis is put forward for motor neglect. When applied to unilateral neglect, it suggests that sensorial signals treated by the right hemisphere do not reach a significant functional level. In such case, the left hemisphere assumed to be dominant for awareness of body and space would receive from the right hemisphere a message interpreted as nul and would neglect information coming from the left.     

Time and neglect: abnormal temporal dynamics in unilateral spatial neglect

Temporality enters our immediate experience as passage and becoming: the role time plays in the construction of a world of enduring entities tends to go unnoticed. This paper examines the relation between time and ontology in the context of unilateral neglect, a neuropsychological syndrome in which patients fail to perceive or respond to stimuli in the contralateral hemifield, behaving as if that half of space does not exist. Traditional models characterize neglect exclusively in spatial terms. Based on recent investigations suggesting abnormal temporal dynamics, here we highlight the impact of time factors on the presentation of the disorder. Neglect patients do not simply miss the presence of stimuli on the left: they also ignore the past as well as the future of neglected stimuli. We claim that, if this occurs, it is because time, and not only space, is impaired.     

Bodily neglect and orientational biases in unilateral neglect syndrome and normal subjects

Patients with neglect erred toward the right when attempting to locate the intercepts of their midsagittal planes with a horizontal line placed in front of them. When control subjects could not see their bodies, they also pointed to the right. While control subjects improved when they were able to see their bodies, neglect subjects did not. When the horizontal line was moved toward the right, both neglect and control subjects increased their rightward pointing errors. However, patients with neglect made greater errors than did controls. When the line was in far left hemispace, controls pointed accurately to their midsagittal planes. The neglect subjects, in contrast, erred toward the left. Our results suggest that patients with neglect from right hemisphere lesions are not only inattentive to their bodies, but are also distracted by extracorporeal stimuli, especially on the right. Our results also suggest that normal subjects have a propensity to orient to or be distracted by stimuli in right hemispace.     

Perceptual and premotor factors of unilateral neglect

Right-brain-damaged patients showing unilateral neglect underwent a specifically devised line-bisection task that allowed uncoupling of the direction of visual attention from that of hand movement. This made it possible to isolate and separately assess perceptual and premotor factors of the disorder. Comparison of experimental and radiologic data suggested that premotor factors were more pronounced in patients with lesions involving the frontal lobes than in patients with lesions confined to postrolandic areas. The technique employed is compatible with bedside examination and provides data useful for standard assessment of neglect symptomatology for both clinical and experimental purposes.     

Double dissociation between unilateral neglect and anosognosia

We report two patients presenting with a subacute right hemisphere stroke. These cases demonstrate a double dissociation between unilateral neglect and anosognosia for hemiplegia. The first patient suffered from a severe left hemiplegia associated with severe and persisting unilateral neglect. He appeared fully aware of his motor impairment. The second patient had a severe left hemiplegia, without any major sign of unilateral neglect on clinical tests nor on behavioural assessment. Nevertheless, he presented a severe and sustained anosognosia for hemiplegia. These case reports support the assumption that anosognosia and unilateral neglect, although they are frequently associated, may rely on independent mechanisms.     

The mechanism of unilateral spatial neglect

We investigated a test for unilateral spatial neglect and discussed the mechanism of this symptom. Seventy eight patients with lesions on the right cerebral hemisphere were examined on line bisection, line cancellation, figure copying, clock drawing and location on the map. The statistical analysis revealed (1) there were no correlations between line bisection and clock drawing or between line bisection and location; (2) those with abnormal results on line bisection were apt to indicate normal results on line cancellation and figure copying, while in line cancellation, figure copying, clock drawing and location, normal results on one task meant normal results on the other. These results indicated clock drawing and location might include different factors from other tasks, line bisection was the most sensitive task for unilateral spatial neglect, and abnormality on line cancellation might be similar to that figure copying. Unilateral spatial neglect may be based on several disorders, and it may be assumed to have several aspects. One of these disorders may be defective searching. Unilateral spatial neglect may be more severe when there is sensory disturbance (hemianopsia) with a searching deficit. Other disorders, such as cognitive disturbance, memory disturbance and so on, may also be associated with unilateral spatial neglect, and it is necessary to consider the versatility of this symptom.     

The multivariate nature of unilateral neglect

Abstract

It is almost certain that unilateral neglect has been observed for centuries. Presumably people have suffered brain injury from the beginning of our existence, yet broad interest in the behavioural phenomena associated with unilateral neglect has appeared relatively recently. So one of the questions surrounding this interest is what new scientific issues have emerged that make the study of neglect so intriguing? It seems to me that the main answer to this question is the renewed interest in cognition and consciousness, and the failure to explain consciousness in biological terms. The magnet that pulls researchers (at least this researcher) into the study of unilateral neglect is the astonishing phenomenology that a person can exhibit both consciousness and unconsciousness of the perceptual scene, perceptual object, or the self at the same moment.     

Experimental remission of unilateral spatial neglect

Over the past several decades a growing amount of research has focused on the possibility of transiently reducing left neglect signs in right brain-damaged patients by using vestibular and/or visuo-proprioceptive stimulations. Here we review seminal papers dealing with these visuo-vestibulo-proprioceptive stimulations in normal controls, right brain-damaged (RBD) patients, and animals. We discuss these data in terms of clinical implications but also with regards to theoretical frameworks commonly used to explain the unilateral neglect syndrome. We undermine the effect of these stimulations on the position of the egocentric reference and extend the notion that the positive effects of these stimulation techniques may stem from a reorientation of attention towards the neglected side of space or from a recalibration of sensori-motor correlations. We conclude this review with discussing the possible interaction between experimental rehabilitation, models of neglect and basic spatial cognition research.     

Grouping influences in unilateral visual neglect

Effects of grouping on unilateral neglect were investigated in 8 neurological patients with right hemisphere damage. It is well documented that arranging items to form a group spanning the midline decreases the magnitude of neglect. In the present study we examined how clusters of groups within the left or right visual field affect neglect and whether isolated groups within the neglected field deflect attention from right-sided displays. We orthogonally varied the strength of grouping on the right and left sides of a display and measured the time to find a predesignated target in one of those groups. Groups on the neglected left side did not affect right-sided target detection any more than an empty left page. However, strength of grouping did affect left sided target detection. These findings are discussed as they relate to attention and preattention in unilateral visual neglect.     

Neurobiology of unilateral spatial neglect.

Hemispatial neglect is a common and disabling consequence of stroke. Earlier studies aimed to identify a single area of the brain where damage caused neglect and sought a single disrupted process that could account for the symptoms. Recent studies have shifted toward identifying component processes and representations underlying spatial attention required for various tasks and identifying areas of the brain responsible for each component that together constitute the network of regions responsible for neglect. This review focuses on recent insights into the mechanisms of neglect, regions of neural dysfunction that cause disruption of particular components or forms of neglect, and potential means of ameliorating neglect. Converging evidence supporting these insights comes from new imaging modalities in acute stroke, functional imaging, transcranial magnetic stimulation, electrophysiological studies in humans, and single-cell recording studies in nonhuman primates.     

Vestibulo-ocular and optokinetic impairments in left unilateral neglect

Right brain damaged patients affected by left unilateral neglect (N+) typically fail to explore the contralesional space. For the first time, this study investigates the dynamic and spatial features of the horizontal vestibular-ocular response (VOR), the optokinetic response (OKR) and the VOR-OKR interaction in six N+ and in five right brain damaged patients without neglect (N-). No lateral asymmetry of the gain (i.e. eye velocity to head velocity ratio) of VOR slow phases was found in either group. In the VOR, N+ had higher frequency of slow-rightward/fast-leftward phases and higher contralesional shift of the beating field (i.e. orbital position of fast phases). In the VOR-OKR, there was an increase of gain in both lateral directions and in both groups even though in N-, there was a lower phase shift between eye and head velocity. In contrast to the VOR, in the VOR-OKR, N+ had higher frequency of slow-leftward/fast-rightward phases. The VOR-OKR interaction also introduced an ipsilesional shift of the beating field in both N+ and N-. In the OKR, N+ showed a drop in the velocity, amplitude and frequency of slow-rightward/fast-leftward phases. These findings potentially suggest that each hemisphere modulates VOR with contralaterally directed slow phases and OKR with ipsilaterally directed slow phases. This organisation could facilitate maintenance or fast recovery of combined VOR + OKR after unilateral brain damage. The same findings suggest that by inducing slow-leftward phases, vestibular and optokinetic stimulation improve left side neglect through the activation of different hemispheric pathways. No ipsilesional deviation of the subjective "straight ahead" was found in N+. These results show that chronic unilateral neglect can be dissociated both from deficits of ipsilesionally directed VOR and from ipsilesional deviation of the subjective midsagittal plane of the body.     

Near and far visual space in unilateral neglect

A 24-year-old right-handed woman with a right temporal hematoma showed marked left visual neglect for far but not near space in a variety of tasks systematically given in near and far distance conditions. This case thus provides the dissociation opposite to Halligan and Marshall's patient, who had neglect for near but not far space after a right parietal stroke. Furthermore, although she made rightward errors in bisecting far-distant lines, our patient made smaller opposite leftward errors for near-distant lines. The evidence that unilateral neglect of far and near visual space may exist independently supports a division in the neural systems subserving attention to different compartments of the extrapersonal space in humans.