Analysis of the Syndrome of Unilateral Neglect

NOTE ANALYSIS OF THE SYNDROME OF UNILATERAL NEGLECT Glynda Kinsella', John Olver2, Kim Ng', Sue Packer' and Richard Stark2 ('Department of Psychology, La Trobe University, Bundoora, Victoria, Australia; 2Department of Neurology and Neurological Rehabilitation, Alfred Hospital, Melbourne, Victoria, Australia)

Considerable effort over the past several years has been directed towards the characterization of prognostic indicators for stroke recovery and functional outcome. Amongst the array of cognitive processes potentially disrupted by stroke, unilateral spatial neglect, or hemi-inattention, has been identified as predictive of poor functional otucome after stroke (Kinsella and Ford, 1980, 1985). Much therapy time is devoted to attempts to remediate the disorder but unfortunately the development of appropriate rehabilitation programmes is hampered by the wide variation in the number and type of tasks used to diagnose neglect. In a recent study on stroke patients Halligan, Marshall and Wade (1989) confirmed through factor analysis a single construct that could explain most of the variance in their selected measures of neglect. This encouraged the description of neglect as predominantly a single phenomenon. This interpretation did not reflect our clinical perception of wide variability in the presentation of neglect patients and also potentially did not reflect some proponents within the theoretical literature who do not discount the potential for modality-specific forms of neglect (Cubelli et aI., 1991; Rizzolatti, 1990). Most of the cognitive models currently used to interpret neglect use an attentional dysfunction theory (Kinsbourne, 1987; Heilman et aI., 1985; Posner et aI., 1984). Posner (1984) argues for a selective deficit in covert orienting of attention to stimuli in extrapersonal space, specifically in the disengage component of orienting behaviour. His series of experimental studies implicate the parietal lobes in this aspect of attentional behaviour. Using this model Posner has been able to demonstrate that provision of a cue in the neglected hemispace effectively moderates the demonstration of neglect, or hemi-inattention. Alternatively a modification of the attentional dysfunction theory, which has been largely elaborated by Bisiach and colleagues (Bisiach, Capitani, Luzzatti et aI., 1981), examines the potential for evoking a distorted internal representation of space to explain the phenomenon of neglect. This model directly addresses the observation that on tasks that require imagery selected neglect subjects will perform as poorly in reporting details on one side of the internal representation, or image, as in their response to stimuli in one half of external space. In other words one side of the internal representation is distorted in cases of neglect. More recent research (Bisiach, Bulgarelli, Sterzi et aI., 1983; Proeve, 1989) has been addressing whether these two models can be combined. Indeed this was suggested by Baddeley and Lieberman (1980) who explained neglect as arising from a deficit in the mechanism that scans the left part of the inner screen to retrieve information and not from damage to the representation itself. This would imply that neglect for stimuli in external space and neglect on imaginal tasks are accounted for by a single attentional model. Whether all neglect patients can be explained in this paradigm or whether there is potential for major dissociations of sub-groups within the neglect syndrome awaits to be seen. Cortex, (1993) 29,135-140

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G. Kinsella and Others EXPERIMENT

1

The general aim of the first study was to assess the potential for heterogeneity in a sample of patients demonstrating neglect. Following the general approach of Halligan, Marshall and Wade (1989) this study evaluates a group of stroke patients in terms of their performance on a variety of common clinical measures of neglect. However, in contrast to Halligan et al. (1989) the assessment tasks that were selected were chosen to address scanning of stimuli in external space and also capacity on tasks requiring access to internal representation of space. By inspecting a factorial analysis of the test data a single, covarying pattern of performance across these tests would provide evidence supporting a single underlying construct of neglect. This would support the work of Halligan et al. (1989). Alternatively our hypothesis proposes that there are potentially at least two basic features, or levels, of neglect - the expected scanning defect of stimuli in external space, and secondarily an alteration in the functioning of the internal representation of space. This leads to the prediction that in individual cases there could be dissociation of deficit, although probably in most cases the impairments will co-exist in varying patterns of severity (cf. Frontal lobe behavioural impairments - loss of emotional control and/or decreased motivation). Materials and Method Subjects

40 patients with a diagnosis of unilateral stroke restricted to the right cerebral hemisphere were recruited from admissions at Caulfield General Medical Centre, Melbourne. The argument for simply looking at right lesioned subjects was for clarity in the model of neglect being developed without the contamination of language disabilty. This is appropriate for a preliminary study but later studies will need to consider left hemisphere contributions. Patients were diagnosed by neurological examination and confirmed by C.T. scan. Exclusions included brainstem lesions, or if there was evidence of additional cerebral dysfunction (e.g. dementia) that would compound the stroke related cognitive impairment. All subjects were right handed and capable of understanding the task requirements. There were 19 males and 21 females. The mean time since the onset of the stroke was 44 days, or about 6 weeks (range 2-12 weeks). Assessments

A neglect battery of 6 tests was given to each patient. These were selected from a larger ongoing neglect study and are representative of measures used within the clinical and research literature. Three of these measures were selected to assess the presumed scanning component of neglect of stimuli in external space: 1. Shape Cancellation Task (Weintraub and Mesulam, 1987). A sheet of paper containing random shapes is placed in front of the subject. The subject in instructed to circle all the target stimuli that he/she can perceive across the page. Scoring: Total omissions, possible range 0-60. 2. Modified Line Bisection Task (Schenkenberg, Bradford and Ajax, 1980). 18 lines are placed across a sheet of paper which is placed in front of the subject. The subject is asked to bisect each of the lines on the page. Scoring: Mean percent deviation, possible range 0-100. 3. Circle Cancellation (Bisiach, Luzzatti, and Perani, 1979). A circle of 12 small circles surrounds a central circle. The subject is instructed to place a line through each of the circles and the central circle is used as a demonstration. Scoring: Total omissions, possible range 0-10 (the upper and lower central circles were omitted for scoring purposes).

The remaining three tasks were used to provide estimates of internal representation of space, or imagery: 4. Landscape Scenery (Gainotti, Messerli and Tissot, 1972). Subjects are asked to reproduce

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a simple drawing of a house, fence, and trees. Scoring: Neglect of elements of the picture, possible range 0-4. 5. Spontaneous Drawings. Subjects are asked to draw from memory a daisy, wagon wheel, person, and clock face. Scoring: Failure to draw elements of the pictures, possible range 0-4. 6. Tactile Maze (De Renzi, Faglioni and Scotti, 1970). A simple wooden maze is placed in front of the subject. He/she is instructed to find the marble (which is placed in one of the arms of the maze) by exploring the maze with his/her finger-tip. After practice the subject is blindfolded and a second maze is placed in front of the subject. They are again instructed to find the marble, but this time without the help of vision. There are 4 trials on the left and 4 trials on the right, of 90 seconds each. Scoring: Total failures to find the marble, possible range 0-8.

Results and Discussion

In order to investigate the inter-relationships between the neglect tasks, a Principal Components Analysis (orthogonal varimax rotation) was carried out on the total stroke data. The rotated factor matrix indicated two factors that accounted for 82.4% of the total variance explained (see Table I). The first factor had significant loadings from all the neglect tasks apart from maze performance. The tasks providing the greatest contribution to the factor were those tasks that were chosen to represent the scanning of stimuli in external space. This factor highlights the importance of this aspect of disorder in a random group of neglect subjects. The tasks required visual scanning of presented stimuli and failure on these tasks is readily understood in terms of a defect in orienting of attention to external space. Interestingly a second factor emerged that consisted of performances on the maze task and secondary contributions from spontaneous drawings and scenery copying i.e. those tasks chosen to address internal representation skills. The maze task is the only task to be timed and as such the second factor could be perceived to represent a central slowing in speed of response. However counter to this interpretation are the secondary significant loadings on Factor 2 from the drawing tasks in the battery. The same argument can be made about the overtly non-visual nature of the maze task. De Renzi et al.'s (1970) original interpretation of performance on the maze suggested that the subject must rely on his/her recollection of the outline of the maze and the already explored areas of the maze in order to achieve a good searching strategy - the task evokes a representational skill, not a simple perception of space. The drawing tasks in this study can be similarly argued to require an arousal of the internally represented stimulus before successful completion of the task. The results of the factorial analysis isolating salient dimensions of neglect may be used to propose sub-groups of patients. Theoretically it would appear from our data that cases could be identified where the deficit pattern consisted mainly of dysfunction on external TABLE I

Varimax Rotated Factor Matrix from the Principal Components Analysis of Results from the Neglect tasks Loading on factor 1 Shape Cancellation Line Bisection Deviation Circle Cancellation Landscape Scenery Spontaneous Drawings Tactile Maze Failures Eigen Value Percentage of Variance

.84 .82 .92 .67 .72 3.84 64.1

Loading on factor 2

.62 .56 .96 1.15 19.2

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scanning tasks or on imaginal tasks. Alternatively many cases will present where the pattern is one of mixed deficit. Identification of these sub-groups requires a clustering of individuals rather than variables. If sub-groups of neglect exist cluster analysis should reveal non-overlapping homogenous groups rather that a relatively uniform distribution of symptoms across patients. Unfortunately this approach was not possible with this data set as the size of the sample could lead to unreliable results.

EXPERIMENT

2

Consequent to our initial findings in the first study we were interested to determine whether the identified factors were capable of predicting functional recovery of stroke patients. Our previous work (Kinsella and Ford, 1980, 1985) had demonstrated that neglect is clearly predictive of poor functional outcome at 3 and 12 months post stroke. However we were interested in refining this relationship and considering whether both of our identified neglect factors were predictive of outcome. Our tentative hypothesis promoted that the factor of disrupted internal representation of space would be more disruptive to daily living activities than the factor of scanning of external stimuli which may be responsive to intervention programmes (Pizzamiglio et aI. , 1990).

Materials and Method In order to address this question we recruited from admissions to Caulfield General Medical Centre a further 27 patients with a diagnosis of unilateral stroke restricted to the right cerebral hemisphere. The same exclusion categories were applied as described before. They were assessed at 2-5 weeks post-stroke, 3 months and 6 months post-stroke. Assessments utilized the previously described neglect battery and the Barthel scale of functional independence (Mahoney and Barthel, 1965) which gives measures of independence in self-care and mobility.

Results and Discussion A correlation matrix was constructed to compare the relationship between the two factors of neglect, as identified in the previous study, and the measures of independence in daily living activities (Self-care and Mobility) at initial assessment, 3 months and 6 months poststroke. It was found that both factors did indeed correlate with fuctional status but there was no significant differential relationship in this respect between the 2 factors and activities of daily living. It is important to note that by 6 months post-stroke the self-care scale of the Barthel rather than the mobility scale was emerging as more strongly related to the initial scores on the neglect factors. We suggest that recovery of motor function is less compromised by the cognitive disorder of neglect than the self-care activities, e.g. cooking, dressing, bathing. This is important when considering provision of rehabilitation programmes and we are currently undertaking a further study to more carefully delineate this relationship. An argument could be made that neglect is associated with an initially more severe stroke and this underwrites the relationship found between neglect and functional independence at 6 months post-stroke. In the absence of discrete neurological imaging of the initial lesions (apart from standard CT scan data) we constructed an index of severity of motor impairment by summating the impairment rating of face/arm/leg as rated by a Consultant of Rehabilitation. This was assessed initially (2-5 weeks), 3 months and 6 months post-stroke and was correlated with the factors of neglect. It was found that none of the correlations between variables even approached significance. We are not arguing that initial severity of motor impairment will not predict functional outcome of stroke patients. Indeed, there is ample evidence demonstrating the powerful relationship between initial motor severity and stroke

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TABLE II

Pearson's Correlations between the Neglect Factors (at initial assessment) and Barthel Scores at Initial, 3 Months and 6 Months Assessment (N=27) Factor I AttentionallScanning

Barthel

Factor 2 Internal representation

-.54* -.46* -.54*

3 months: Self Care Mobility Total

-.44* -.45* -.49 -.52* -.53* -.55*

6 months: Self Care Mobility Total

-.72** -.55* -.63**

-.70** -.53** -.63**

Initial test: Self Care Mobility Total

*p <

.01;

** P <

-.59** -.58** -.60**

.001.

outcome (Lincoln et aI., 1989). However, we are making the point that neglect in a stroke patient is not simply explained as a correlate of severity of motor impairment but independently contributes to functional recovery post-stroke. A larger data set is now needed to assess the inter-relationship and prediction equation of these and other variables as they relate to stroke recovery. Research to date using large data sets have not included careful documentation of the neglect syndrome, often confining their assessment to noting extinction on double simultaneous stimulation tasks. Our data failed to differentiate the factors in their power to predict functional independence in the stroke patients at 6 months. This may reflect the lack of systematic programmes of rehabilitation directed towards alleviating neglect that these patients were exposed to. Further intervention studies are indicated to determine whether it is possible to alter this equation. GENERAL DISCUSSION

The results of these studies encourage the view that hemi-inattention is a complex syndrome and subjects identified as suffering from the disorder can vary in systematic dimensions. The Principal Components Analysis confirmed our hypotheses that there are at least two potential factors contributing to the neglect syndrome - an external scanning factor and a disrupted internal representation of space. It is anticipated that most commonly these factors will co-exist and form the classical neglect syndrome. However, theoretically the symptoms, or levels of neglect, could be observed to occur separately. Our identified neglect factors were significantly related to functional independence achieved in a group of stroke patients at 6 months post-stroke. Neglect was particularly disruptive in the domain of self-care activities but not so strongly related in the area of mobility. This has implications for the rehabilitation programmes required by this particular group of stroke patients. The statistical results from this study are tentative and require replication with larger samples or single case analysis. However the data provides encouragement to look for dissociations in the neglect syndrome. Divergent theoretical models can be more easily accomodated within this frame of the disorder. The data are also critical when considering management. The clearer that the contributing bases to neglect can be delineated the greater the possibility that targeted, specific remediation programmes can be developed and evaluated. Imaginal/representational difficulties in the neglect syndrome could be hypothesized to be less tractable to retraining and this may provide a basis for predicting those subjects who cannot make clear gains from rehabilitation based on attentional cueing. If these cases are contrasted in terms of recovery over time then this information will contribute to a clearer base for intervention and management. Prediction of post-stroke functional recovery will be improved.

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C. Kinsella and Others ABSTRACT

Using a variety of clinical measures of unilateral neglect 40 right hemisphere lesioned stroke subjects were compared in terms of neuropsychological deficit. The results of the study encourage the view that unilateral neglect is a complex syndrome and subjects who indicate the disorder may vary in systematic dimensions. There are at least two factors contributing to the neglect syndrome - a scanning factor of external stimuli and a disrupted internal representation of space factor. Both the obtained factors were correlated with functional independence at 6 months post-stroke in a further group of 27 right hemisphere lesioned stroke patients. It is probable that most commonly these factors co-exist and form the classical neglect syndrome but theoretically they may occur separately and this leads to implications for management. Acknowledgements. The study was supported by an Alfred Hospital Research Fellowship. The authors would like to thank the subjects for their participation in the study.

REFERENCES

BADDELEY, AD., and LIEBERMAN, K. Spatial working memory, In M.I.Posner and O.S.M. Marin (Eds.), Attention and Performance V/lI, Hillsdale, NJ: Erlbaum, 1980, pp. 521-539. BISIACH, E., BULGARELLI, C., STERZI, R. , and V ALLAR, G. Line bisection and cognitive plasticity of unilateral neglect of space. Brain and Cognition, 2: 32-38, 1983. BISIACH, E., LUZZATTI, C., and PERANI, D. Unilateral neglect, representational schema and consciousness. Brain, 102: 609-618, 1979. BISIACH, 8., CAPrrANI, E., L UZZATTI, C., and PERANI, D. Brain and conscious representation of outside reality. Neuropsychologia, 19: 543-551, 1981. CUBELLI, R. , NICHELLI, P., BONITO, V., DE TANTI, A, and INZAGHJ, M . Different patterns of dissociation in Unilateral neglect. Brain and Cognition, 15: 139-159, 1991. DE RENZI, E., FAGLIONI, P., and SCOTTI, G. Hemispheric contribution to exploration of space through the visual and tactile modality. Cortex, 6: 191-203, 1970. GAINOTTI, G., MESSERLI, P., and TISSOT, R. Qualitative analysis of unilateral spatial neglect in relation to laterality of cerebral lesions. Journal of Neurology, Neurosurgery and Psychiatry, 35: 545-550, 1972. HALLIGAN, P.W., MARSHALL, J.e. , and WADE, D.T. Visuospatial neglect: Underlying factors and test sensivity. The Lancet, October 14: 908-911, 1989. KINSBOURNE, M. Mechanisms of unilateral neglect. In M. Jeannerod (Ed.), Neurophysiological and Neuropsychological Aspects of Spatial Neglect, North-Holland: Elsevier Science Publischers B.V., 1987. KI NSELLA, G. , and FORD, B. Acute recovery patterns in stroke patients: Neuropsychological factors. The Medical Journal of Australia, 2: 663-666, 1980. KINSELLA, G., and FORD, B. Hemi-inattention and the recovery patterns of stroke patients. International Rehabilitation Medicine, 7: 102-106, 1985. MAHONEY, F.I., and BARTHEL, D.W. Functional evaluation: Barthel index. Md. State Med. J., 14: 6165, 1965. R1ZZ0LATTI, G., and CAMARDA, R. Neural circuits for spatial attention and unilateral neglect. In M . Jeannerod (Ed.), Neruphysiological and Neuropsychological Aspects of Spatial Neglect. Amsterdam: Elsevier Science, 1987, pp. 298-313. POSNER, M.I., WALKER, J.A, FRIEDRICH, F.A, and RAFAL, R.D. Effects of parietal lobe injury on convert orienting of visual attention. Journal of Neuroscience, 4: 1863-1974, 1984. PROEVE, M. Cueing in hemi-inattention. Unpublished Master of Psychology Thesis, La Trobe University, Melbourne, Australia, 1989. RIZZOLATTI, G., and BERTI, A. Neglect as a neural representation deficit. Revue Neurologique (Paris), 146: 626-634, 1990. SCHENKENBERG, T., BRADFORD, D .C. , and AJAX, E.T. Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology, 30: 509-517, 1980. WEINTRAUB, S., and MESULAM, M .M. Right cerebral dominance in spatial attention: Further evidence based on ipsilateral neglect. Archives of Neurology, 44: 621-625, 1987.

Dr. Glynda Kinsella, Department of Psychology, La Trobe University, Bundoora, Victoria 3038, Australia.