Brain (1979), 102, 609-618
UNILATERAL NEGLECT, REPRESENTATIONAL SCHEMA AND CONSCIOUSNESS by EDOARDO BISIACH, CLAUDIO LUZZATTI and DANIELA PERANI
INTRODUCTION
of unilateral neglect cluster into three main groups, these being classified by reference to the level of function to which one chooses to allocate the disorder from which the behavioural manifestations proceed. First, some authors have argued that the syndrome is the result of an interruption, attenuation, or lack of synthesis in the flow of information conveyed to one hemisphere. The study by Denny-Brown, Meyer and Horenstein (1952) is the most representative of such stimulus-bound theories, among which can also be found Bender's explanation in terms of extinction phenomena {see Bender, 1977, for a comprehensive account). On the same (physiological) level, unilateral neglect has more recently been regarded as the one-sided breakdown of mechanisms subserving the 'orienting response' to incoming stimulations {see Heilman and Watson, 1977). These theories evolved contemporaneously with a second and different approach, which took into account the representational map which underlies the organization of perceptions and actions: the concept of'body schema' so insistently referred to in the literature on unilateral neglect is a classical instance thereof. A third, psychodynamic, line of reasoning suggests motivational explanations for some phenomena of the syndrome (Zingerle, 1913; Schilder, 1935; Weinstein and Kahn, 1955). The plausibility of hypotheses of this third kind will not be argued here. Physiological theories owe much of their appeal to the apparent 'objectiveness' of the mechanisms to which unilateral neglect is reduced; they seemingly dispense with the need to resort to dubious psychological constructs like 'body schema', 'representational space', etc. The concept of body schema was introduced into clinical neurology at the beginning of the century (Wernicke, 1900; Hartmann, 1902; Bonnier, 1905; Pick, 1908; and others) and was subsequently developed by Head and Holmes (1911). Since then it has often been invoked as a clue to the understanding of manifold neurological disorders, including unilateral neglect (Brain, 1941; Gerstmann, 1942; Lhermitte, 1942; THEORIES
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on June 16, 2014
(From the Centro di Neuropsicologia delFUniversita di Milano, Milan 20122)
610
EDOARDO BISIACH AND OTHERS
We now present a new piece of evidence which undermines those theories which seek to explain unilateral neglect in terms of a diagram of input-output connectivities. In our opinion this evidence also helps towards an improved conception of the essential structure of the central 'representational schema' whose disorder results in unilateral neglect. Our experiments show that in patients with unilateral brain lesions, forms reconstructed by the temporal integration of successive visual stimuli appearing in a stationary, vertical slit are neglected unilaterally.
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on June 16, 2014
Roth, 1949; Critchley, 1953; and others). As such, however, its force was in most instances not compelling, so that it could be easily disregarded by upholders of other theories. Some reasons for this weakness may be pointed out. Even in Head and Holmes' classical formulation, the structure and function of the schema are far from being exhaustively and unambiguously described. Multiple corporeal schemata are postulated, of which the unifying principle remains obscure. It is not even clear what changes, if any, are to be expected in the schemata after interruption of the sensory inflow at various levels. Subsequent analyses (Lhermitte, 1942) failed to bring major improvements to the concept. A feature common to all these attempts at interpreting the syndrome of unilateral neglect in terms of a disordered schema, and which appears to account for their limited usefulness, is a certain reluctance to enlarge the analysis beyond mere corporeal representation. This is all the more striking when one remembers that conspicuous disorders of behaviour in extra-corporeal hemi-space are no less characteristic of the syndrome than the neglect of one half of the body. But the chief fault of schema-inspired accounts of unilateral neglect is, perhaps, that they have generally misused the concept of schema to describe a set of disorders, rather than arguing its necessity as an explanatory construct. Though at an advantage conferred by the relative weakness of psychological interpretations, physiological theories are also open to criticism. Denny-Brown et al. (1952) for instance, having epitomized the features of the sensory defect ensuing from the parietal lesion of their patient, concluded that 'the very striking change in the general behaviour of the patient, namely her failure to attend to the left side of her body or of space can also be viewed as a disturbance of synthesis of multiple sensory data'. The supposed causal relationship between sensory disorders and unilateral neglect, however, is objectionable on both logical and empirical grounds: loss of information, in fact, does not imply cessation of the search for information, and it is undeniable that sensory disorders at any level do not, as a rule, appear in association with neglect phenomena. Though more satisfactory, the explanation in terms of 'orienting response' which was suggested by Heilman and Watson (1977) fails, like all physiological theories, to account for some of the most essential features of the syndrome. None of these theories are indeed of much use when faced with facts such as the defective blind exploration of the neglected hemi-space by the contralateral, unaffected hand (De Renzi, Faglioni and Scotti, 1970), or the one-sided omission of details from verbal descriptions of remembered scenes (Bisiach and Luzzatti, 1978).
UNILATERAL NEGLECT
611
As the investigation was primarily addressed to unilateral neglect per se, leaving aside the question of inter-hemispheric differences, and in order to avoid any complication by aphasia, the study was restricted to patients with right-sided brain damage.
MATERIALS AND METHODS Subjects
Stimuli and Procedure The subjects were required to detect differences occurring within pairs of patterns successively presented at intervals. These were random, white cloud-like shapes, 20 cm wide and 6 cm high, lying on a blue background. A central sector 10 cm wide was common to all patterns, while the left and right lateral sectors were varied, thus forming three identical pairs, three pairs differing on the left, and three on the right. Nine more pairs were obtained by mirror reversal. Stimuli were presented by means of a Fairchild Mark VI Super-8 Sound Projector placed approximately 50 cm in front of the subject. In the first part of the experiment (static exposure), each pattern figuring a pair was shown for 2 s with a 1 s black interstimulus interval. The 18 pairs followed one another at 5 s intervals. In the second part (dynamic exposure), the screen was blacked out with the exception of a central vertical 1.5 x 12 cm slit, which allowed a partial view of the stimulus at each moment. The patterns moved from left to right, or vice versa, at a speed of 10 cm per second. The complete transit of a single pattern behind the slit took, therefore, 2 s. The second pattern of the pair, moving in the same direction as the former, started its transit after a 1 s interstimulus interval. Each of the 18 pairs of stimuli were shown in both left- and rightward motion (non-contiguous trials, that is, the rightward transit of a given pair did not follow immediately on the leftward transit of that pair), hence the second part of the experiment consisted of 36 trials, with 5 s intertrial intervals. In both parts of the experiment, pairs of patterns were arranged to follow a fixed, random schedule. Care was, however, taken to ascertain that trials differing on the left and trials differing on the right would not cluster, thus eliminating the possibility of spurious right-left gradients of difference-detections due to fatigue. Subjects were not asked to specify on which side the detected differences occurred. Responses were recorded after each trial and subjects were not informed as to their accuracy.
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on June 16, 2014
The subjects of the experiment were 19 right brain-damaged patients showing signs of unilateral neglect (fig. 1). In order to qualify for selection the subjects had to satisfy the following criteria: (a) clinical and instrumental evidence of a lesion confined to the right hemisphere, and (b) one or more left-sided omissions in crossing out 13 circles in a 23 x 18 cm display. The circles, three in each quadrant, had a diameter of 1 cm and were symmetrically arranged around a central one, which formed the starting point of the task. Three patients were suffering from a brain tumour (C.P., A.C. and A.G.); the other 16 had recently sustained a cerebrovascular attack. Fig. 1 shows the locus and extent of the lesions reconstructed from CT scans (Luzzatti, Scotti and Gattoni, 1979); the data of two of the patients are missing as they were admitted to another hospital. With the exception of V.P., all the patients had a left hemiparesis and a left somatosensory disorder ranging from mild to severe. All had a more or less severe left visual field defect, detected on confrontation. Ocular movements on verbal command, ocular tracking movements and optokinetic nystagmus were examined in 16 of the patients (the missing data are those of T.M., E.G. and M.Z.); they were variously disordered in all these patients except V.P., G.B. and V.M. The control group was formed by 30 patients without past or present evidence of any disease involving the nervous system above the cervical cord. The mean age was 66.40 ±6.00 years in the brain-damaged patients and 64.58 + 7.88 in the controls.
612
EDOARDO BISIACH AND OTHERS
T.M.
M.Z.
N.V.
G.B.
D.B.
A.L.
I.M.
L.P.
A.C.
C.S.
V.P.
G.S.
1
A.G. Deep lesion
HHm Superficial lesion H i l Deep + superficial lesion '1~:- Oedema B.B. FIG. 1. Locus and extent of lesions in brain-damaged patients. Maps reconstructed from CT scans (Luzzatti el al., 1979).
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on June 16, 2014
E.G.
UNILATERAL NEGLECT
613
RESULTS
In Table 1 the scores of correct difference-detections on the left (DDL) and on the right side (DDR) of static patterns are shown. The right-left gradient
TABLE 1. STATIC PATTERNS
Mean DDL and DDR Group Control Brain-damaged-
DDL* 3.60 1.37
DDR* 4.10 4.58
(DDR-DDL) was found to differ significantly between the patients and the control group (t (47) = 6.26, P < 0.0001). The data related to dynamic patterns are shown in Table 2, where separate scores for left- and rightward trials are given. From these
TABLE 2. DYNAMIC PATTERNS
Mean DDL and DDR in Left- and Rightward Conditions Group Control Brain-damaged
DDL* Leflw. 2.40 1.58
DDL* Rightw. 3.40 2.47
DDR* Leflw. 3.20 3.10
DDR* Rightw. 2.40 2.16
Maximum scores = 6.00.
scores, the effects of Side, Recency and Direction of the patterns' movement were calculated as shown in Table 3. A 3-variate, one-way analysis of variance (Anderson, 1958) showed that the overall between-groups difference due to these effects was significant (F (3, 45) = 3.338, P = 0.027). Multiple comparisons were therefore carried out in order to test the three effects separately (Roy and Bose, 1953; this method yields theta-points derived from the generalized beta-distribution, which
TABLE 3. DYNAMIC PATTERNS
Effect of Side, Recency and Direction of Movement on the Detection of Differences Group Control Brain-damaged 1 2 3
Side' -0.20 + 1.21
Recency2 + 1.80 + 1.83
Direction of Movement3 +0.20 -0.05
(DDR leftw.+ DDR rightw.)-(DDL leftw. + DDR rightw.). (DDL rightw. + DDR leftw.)-(DDL leftw.+ DDR rightw.). (DDL rightw.+ DDR rightw.)-(DDL leftw.+ DDR leftw.).
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* Maximum scores = 6.00.
614
EDOARDO BISIACH AND OTHERS
could here be converted into points of the F-distribution). The effect of Side was thus found to be significantly different in controls and brain-damaged patients (F (3, 45) = 3.097, P — 0.036) whereas the differences concerning the other two effects were far from being significant (F (3, 45) < 1). DISCUSSION
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We begin by making some preliminary remarks with regard to dynamic patterns. Differences on the left halves of these patterns were more apt to be overlooked by our patients than by subjects in the control group: an overall left/right gradient of performance is apparent in the patients, even if in the case of rightward moving patterns this is counteracted by the strong recency effect, which affected equally the performance of both patients and controls. Actually, the patients scored better on the left, rather than the right half of rightward moving patterns (the former being the last half perceived) but it is important to notice that the difference is not as pronounced as in controls. Oculomotor disorders were present in 81.24 per cent of our patients, a finding which is in agreement with Hecaen's (1962) data on the association of these disorders with unilateral neglect. The hypothesis that oculomotor disturbances might somehow have affected the performance of our patients seems to lack validity as the effect of the direction of moving patterns is negligible. This hypothesis is further undermined by the fact that in the three patients who did not show oculomotor disorders the mean Side effect ( + 1.00) was of the same order as that found in the entire group of patients. Taking all this into consideration, it would appear to be reasonably safe to make a further analysis of the experimental results in terms of unilateral neglect. Though the data of dynamic patterns can better develop our argument, we think that even the most obvious phenomena of unilateral neglect as those witnessed in the first part of the experiment would claim the primary explanatory role of a representational disorder. This would, however, require the assumptions that (a) the nervous system cannot conceivably be programmed to gather information without recruiting an inner model of the source thereof, and (b) that any unmonitored failure in performing the programme implies a breakdown of the model itself. To state this in simpler terms, we think that in the cases of patients like ours the loss of sensory information about one side of space could be easily remedied through exploratory activity initiated by the intact neural structures, if all expectations relative to that side of space were not lacking as a result of the lesion. The incorrigibility of this state even by external pressures, which can be observed in most pronounced cases of unilateral neglect, would suggest that the left side of space has not disappeared from consciousness owing to an Amnesie der linken Seite (Zingerle, 1913). On the contrary, we would suggest that in these instances the actual possibility of conceptualizing the existence of a left side is in fact precluded. In any case, a primary disorder of the spatial schema subtending mental representations is selfevident in the second part of the experiment. All spatial features of the patterns
UNILATERAL NEGLECT
615
The same conclusion had been reached with reference to left-sided omissions from verbal descriptions of remembered perspectives (Bisiach and Luzzatti, 1978). Hence it is likely that the same spatial schema is involved in the two instances, even though the source of the processed information is different. Pylyshyn (1973) has warned against possible misuses of the phenomenological concept of 'image' as an explanatory construct in psychological theories. He states that visual representations are 'much closer to being a description of the scene than a picture of it'. None the less, our findings suggest that the spatial attributes of representations cannot be accounted for solely in terms of propositional retrieval: their left side fades in consequence of right hemisphere impairment, so that their spatial schema appears to be mapped across the brain. Non-localizationistic views of conscious brain activity, of which one of the most intriguing up-to-date developments is holographic models (Pribram, 1971, 1972, 1977; Pribram, Nuwer and Baron, 1974), must face the weight of this evidence afforded by unilateral neglect, even though the major manifestations of the latter are so amazingly ephemeral. Finally, the crucial share of the right hemisphere in the structuring of the representational schema in question does not support existing claims which by mistaking consciousness as being the ability to communicate the contents thereof verbally confine it to the left hemisphere of the brain (Eccles, 1976; Popper and Eccles, 1977; Weimer, 1977). On a more general ground, it is not possible in our opinion to accommodate the data in question by interactionistic theories of mind {see Popper and Eccles, 1977). A mind, not co-extensive with part of the brain, would of necessity be endowed with its own invulnerable model of the world if it were to be able to read out from nervous activity and act on it coherently. Accordingly, it would not endorse the
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shown in the first part were in fact simultaneously displayed and invariant throughout the time of each individual exposure. Some of them might fall into the unattended visual field of brain-damaged patients and be neglected. By contrast the same configurations, when appearing behind the slit, were delineated by a narrow, ever-changing section. Instead of a direct, isomorphic (at least in its earliest stages), neural correlate of their entire shape, it is conceivable that under these viewing conditions, a temporally structured pattern of excitation took place in those formations which subserve vision in proximity to the vertical meridian of the visual field. In order to perceive a moving cloud under these conditions it becomes necessary to effect a translation from an objective temporal dimension into a representational spatial one. Our findings suggest that also the left side of this kind of graph drawn in a merely representational space may to some extent fade into unilateral neglect. It is worth emphasizing that under these viewing conditions no inattention to parts of stimuli occurs and that unilateral neglect affects the internal representations of these stimuli manifesting itself in the left side of the reconstructed cloud, irrespective of whether this side refers to its leading or trailing edge. A topological relationship, therefore, seems to link to the neural substrate the spatial schema where these percepts take shape.
616
EDOARDO BISIACH AND OTHERS
oblivion of one side of the world, even less that of the representational world. On the contrary, it would counteract oblivion by resorting immediately to the surviving neural structures, which would be potentially quite adequate to overcome the defect. This is, in fact, the interactionist's expectation, as expressed by Popper: '. . . the liaison brain is, as it were, almost an object of choice of the selfconscious mind. That is to say, if a certain part of the brain is not available, the self-conscious mind will seek another part as substitute.' (loc. cit., p. 495) which is refuted by the syndrome of unilateral neglect.
SUMMARY .
ACKNOWLEDGEMENT Research supported by CNR Grant CT7701246.
REFERENCES ANDERSON, T. W. (1958) An Introduction to Muliivariate Statistical Analysis. New York: John Wiley. BENDER, M. B. (1977) Extinction and other patterns of sensory interaction. In: Hemi-inattention and Hemisphere Specialization. Edited by E. A. Weinstein and R. P. Friedland. New York: Raven Press, pp. 107-110. BISIACH, E. and LUZZATTI, C. (1978) Unilateral neglect of representational space. Cortex, 14, 129-133. BONNIER, P. (1905) L'aschematie. Revue Neurologique, 12, 605-609. BRAIN, W. R. (1941) Visual disorientation with special reference to lesions of the right cerebral hemisphere. Brain, 64, 244-272. CRITCHLEY, M. (1953) The Parietal Lobes. New York: Hafner. DENNY-BROWN, D., MEYER, J. S. and HORENSTEIN, S. (1952) The significance of perceptual rivalry
resulting from parietal lesion. Brain, 75, 433-471. DE RENZI, E., FAGUONI, P. and Scorn, G. (1970) Hemispheric contribution to exploration of space through the visual and tactile modality. Cortex, 4, 191-203. ECCLES, J. C. (1976) Brain and free will. In: Consciousness and the Brain. Edited by G. G. Globus, G. Maxwell and I. Savodnik. New York: Plenum Press, pp. 101-121.
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Right brain-damaged patients with unilateral neglect were asked to detect differences within pairs of patterns moving left- or rightward behind a narrow vertical slit. It was seen that differences occurring on the left side of the mentally reconstructed images were less easily detected; therefore it is suggested that a representational disorder plays a primary role in unilateral neglect. In the light of these findings, it is possible to take into consideration some implications of unilateral neglect for theories of conscious brain activity.
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GERSTMANN, J. (1942) Problem of imperception of disease and of impaired body territories with organic lesions. Archives of Neurology and Psychiatry, 48, 890-913. HARTMANN, F. (1902) Quoted by H. Zingerle. HEAD, H. and HOLMES, G. (1911) Sensory disturbances from cerebral lesions. Brain, 34, 102-254. HECAEN, H. (1962) Clinical symptomatology in right and left hemispheric lesions. In: Interhemispheric Relations and Cerebral Dominance. Baltimore: Johns Hopkins Press, pp. 215-243.
LHERMITTE, M. J. (1942) De l'image corporelle. Revue Neurologique, 74, 20-38. LUZZATTI, C , SCOTTI, G. and GATTONI, A. (1979) Further suggestion for intracranial localization. Cortex. In press. PICK, A. (1908) Quoted by Friedland, R. P. and Weinstein, E. A. (1977). In: Hemi-inattention and Hemisphere Specialization. Edited by E. A. Weinstein and R. P. Friedland. New York: Raven Press, pp. 1-31. POPPER, K. R. and ECCLES, J. C. (1977) The Self and Its Brain. Berlin: Springer. PRIBRAM, K. H. (1971) Languages of the Brain: Experimental Paradoxes and Principles in Neuropsychology. Englewood Cliffs, New Jersey: Prentice-Hall. (1972) Some dimensions of remembering: Steps toward a neuropsychological model of memory. In: Macromolecules and Behavior. Edited by J. Gaito. New York: AppletonCentury-Crofts, Chapter 17. ——
(1977) Some comments on the nature of the perceived universe. In: Perceiving, Acting and Knowing. Edited by R. Shaw and J. Bransford. Hillsdale, New Jersey: Lawrence Erlbaum, pp. 83-101. NUWER, M. and BARON, R. (1974) The holographic hypothesis of memory structure in brain function and perception. In: Contemporary Developments in Mathematical Psychology. Edited by R. C. Atkinson, D. H. Krantz, R. C. Luce and P. Suppes. San Francisco: Freeman, pp. 416-457.
PYLYSHYN, Z. W. (1973) What the mind's eye tells the mind's brain: A critique of mental imagery. Psychological Bulletin, 80, I -24. ROTH, M. (1949) Disorders of the body image caused by lesions of the right parietal lobe. Brain, 72, 89-111. ROY, S. N. and BOSE, R. C. (1953) Simultaneous confidence interval estimation. Annals of Mathematical Statistics, 24, 513-536. SCHILDER, P. (1953) Quoted by Friedland, R. P. and Weinstein, E. A. (1977). In: Hemi-inattention and Hemisphere Specialization. Edited by E. A. Weinstein and R. P. Friedland. New York: Raven Press, pp. 1-31.
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HEILMAN, K. M. and WATSON, R. T. (1977) The neglect syndrome—a unilateral defect of the orienting response. In: Lateralization in the Nervous System. Edited by S. Hamad, R. W. Doty, L. Goldstein, J. Jaynes and G. Krauthamer. New York: Academic Press, pp. 285-302.
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WEIMER, W. B. (1977) A conceptual framework for cognitive psychology: Motor theories of mind. In: Perceiving, Acting and Knowing. Edited by R. Shaw and J. Bransford. Hillsdale, New Jersey: Lawrence Erlbaum, pp. 267-311. WEINSTEIN, E. A. and KAHN, R. L. (1955) Denial of Illness. Springfield, Illinois: Charles C. Thomas. WERNICKE, K. (1900) Quoted by Zingerle, H. (1913). ZINGERLE, H. (1913) Ueber Stoerungen der Wahrnehmung des eigenen Koerpers bei organischen Gehirnerkrankungen. Monatschrift fur Psychiatrie und Neurologie, 34, 13-36. (Received June 22, 1978)
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UNILATERAL NEGLECT, REPRESENTATIONAL SCHEMA AND CONSCIOUSNESS by EDOARDO BISIACH, CLAUDIO LUZZATTI and DANIELA PERANI
INTRODUCTION
of unilateral neglect cluster into three main groups, these being classified by reference to the level of function to which one chooses to allocate the disorder from which the behavioural manifestations proceed. First, some authors have argued that the syndrome is the result of an interruption, attenuation, or lack of synthesis in the flow of information conveyed to one hemisphere. The study by Denny-Brown, Meyer and Horenstein (1952) is the most representative of such stimulus-bound theories, among which can also be found Bender's explanation in terms of extinction phenomena {see Bender, 1977, for a comprehensive account). On the same (physiological) level, unilateral neglect has more recently been regarded as the one-sided breakdown of mechanisms subserving the 'orienting response' to incoming stimulations {see Heilman and Watson, 1977). These theories evolved contemporaneously with a second and different approach, which took into account the representational map which underlies the organization of perceptions and actions: the concept of'body schema' so insistently referred to in the literature on unilateral neglect is a classical instance thereof. A third, psychodynamic, line of reasoning suggests motivational explanations for some phenomena of the syndrome (Zingerle, 1913; Schilder, 1935; Weinstein and Kahn, 1955). The plausibility of hypotheses of this third kind will not be argued here. Physiological theories owe much of their appeal to the apparent 'objectiveness' of the mechanisms to which unilateral neglect is reduced; they seemingly dispense with the need to resort to dubious psychological constructs like 'body schema', 'representational space', etc. The concept of body schema was introduced into clinical neurology at the beginning of the century (Wernicke, 1900; Hartmann, 1902; Bonnier, 1905; Pick, 1908; and others) and was subsequently developed by Head and Holmes (1911). Since then it has often been invoked as a clue to the understanding of manifold neurological disorders, including unilateral neglect (Brain, 1941; Gerstmann, 1942; Lhermitte, 1942; THEORIES
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on June 16, 2014
(From the Centro di Neuropsicologia delFUniversita di Milano, Milan 20122)
610
EDOARDO BISIACH AND OTHERS
We now present a new piece of evidence which undermines those theories which seek to explain unilateral neglect in terms of a diagram of input-output connectivities. In our opinion this evidence also helps towards an improved conception of the essential structure of the central 'representational schema' whose disorder results in unilateral neglect. Our experiments show that in patients with unilateral brain lesions, forms reconstructed by the temporal integration of successive visual stimuli appearing in a stationary, vertical slit are neglected unilaterally.
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on June 16, 2014
Roth, 1949; Critchley, 1953; and others). As such, however, its force was in most instances not compelling, so that it could be easily disregarded by upholders of other theories. Some reasons for this weakness may be pointed out. Even in Head and Holmes' classical formulation, the structure and function of the schema are far from being exhaustively and unambiguously described. Multiple corporeal schemata are postulated, of which the unifying principle remains obscure. It is not even clear what changes, if any, are to be expected in the schemata after interruption of the sensory inflow at various levels. Subsequent analyses (Lhermitte, 1942) failed to bring major improvements to the concept. A feature common to all these attempts at interpreting the syndrome of unilateral neglect in terms of a disordered schema, and which appears to account for their limited usefulness, is a certain reluctance to enlarge the analysis beyond mere corporeal representation. This is all the more striking when one remembers that conspicuous disorders of behaviour in extra-corporeal hemi-space are no less characteristic of the syndrome than the neglect of one half of the body. But the chief fault of schema-inspired accounts of unilateral neglect is, perhaps, that they have generally misused the concept of schema to describe a set of disorders, rather than arguing its necessity as an explanatory construct. Though at an advantage conferred by the relative weakness of psychological interpretations, physiological theories are also open to criticism. Denny-Brown et al. (1952) for instance, having epitomized the features of the sensory defect ensuing from the parietal lesion of their patient, concluded that 'the very striking change in the general behaviour of the patient, namely her failure to attend to the left side of her body or of space can also be viewed as a disturbance of synthesis of multiple sensory data'. The supposed causal relationship between sensory disorders and unilateral neglect, however, is objectionable on both logical and empirical grounds: loss of information, in fact, does not imply cessation of the search for information, and it is undeniable that sensory disorders at any level do not, as a rule, appear in association with neglect phenomena. Though more satisfactory, the explanation in terms of 'orienting response' which was suggested by Heilman and Watson (1977) fails, like all physiological theories, to account for some of the most essential features of the syndrome. None of these theories are indeed of much use when faced with facts such as the defective blind exploration of the neglected hemi-space by the contralateral, unaffected hand (De Renzi, Faglioni and Scotti, 1970), or the one-sided omission of details from verbal descriptions of remembered scenes (Bisiach and Luzzatti, 1978).
UNILATERAL NEGLECT
611
As the investigation was primarily addressed to unilateral neglect per se, leaving aside the question of inter-hemispheric differences, and in order to avoid any complication by aphasia, the study was restricted to patients with right-sided brain damage.
MATERIALS AND METHODS Subjects
Stimuli and Procedure The subjects were required to detect differences occurring within pairs of patterns successively presented at intervals. These were random, white cloud-like shapes, 20 cm wide and 6 cm high, lying on a blue background. A central sector 10 cm wide was common to all patterns, while the left and right lateral sectors were varied, thus forming three identical pairs, three pairs differing on the left, and three on the right. Nine more pairs were obtained by mirror reversal. Stimuli were presented by means of a Fairchild Mark VI Super-8 Sound Projector placed approximately 50 cm in front of the subject. In the first part of the experiment (static exposure), each pattern figuring a pair was shown for 2 s with a 1 s black interstimulus interval. The 18 pairs followed one another at 5 s intervals. In the second part (dynamic exposure), the screen was blacked out with the exception of a central vertical 1.5 x 12 cm slit, which allowed a partial view of the stimulus at each moment. The patterns moved from left to right, or vice versa, at a speed of 10 cm per second. The complete transit of a single pattern behind the slit took, therefore, 2 s. The second pattern of the pair, moving in the same direction as the former, started its transit after a 1 s interstimulus interval. Each of the 18 pairs of stimuli were shown in both left- and rightward motion (non-contiguous trials, that is, the rightward transit of a given pair did not follow immediately on the leftward transit of that pair), hence the second part of the experiment consisted of 36 trials, with 5 s intertrial intervals. In both parts of the experiment, pairs of patterns were arranged to follow a fixed, random schedule. Care was, however, taken to ascertain that trials differing on the left and trials differing on the right would not cluster, thus eliminating the possibility of spurious right-left gradients of difference-detections due to fatigue. Subjects were not asked to specify on which side the detected differences occurred. Responses were recorded after each trial and subjects were not informed as to their accuracy.
Downloaded from http://brain.oxfordjournals.org/ at Université Laval on June 16, 2014
The subjects of the experiment were 19 right brain-damaged patients showing signs of unilateral neglect (fig. 1). In order to qualify for selection the subjects had to satisfy the following criteria: (a) clinical and instrumental evidence of a lesion confined to the right hemisphere, and (b) one or more left-sided omissions in crossing out 13 circles in a 23 x 18 cm display. The circles, three in each quadrant, had a diameter of 1 cm and were symmetrically arranged around a central one, which formed the starting point of the task. Three patients were suffering from a brain tumour (C.P., A.C. and A.G.); the other 16 had recently sustained a cerebrovascular attack. Fig. 1 shows the locus and extent of the lesions reconstructed from CT scans (Luzzatti, Scotti and Gattoni, 1979); the data of two of the patients are missing as they were admitted to another hospital. With the exception of V.P., all the patients had a left hemiparesis and a left somatosensory disorder ranging from mild to severe. All had a more or less severe left visual field defect, detected on confrontation. Ocular movements on verbal command, ocular tracking movements and optokinetic nystagmus were examined in 16 of the patients (the missing data are those of T.M., E.G. and M.Z.); they were variously disordered in all these patients except V.P., G.B. and V.M. The control group was formed by 30 patients without past or present evidence of any disease involving the nervous system above the cervical cord. The mean age was 66.40 ±6.00 years in the brain-damaged patients and 64.58 + 7.88 in the controls.
612
EDOARDO BISIACH AND OTHERS
T.M.
M.Z.
N.V.
G.B.
D.B.
A.L.
I.M.
L.P.
A.C.
C.S.
V.P.
G.S.
1
A.G. Deep lesion
HHm Superficial lesion H i l Deep + superficial lesion '1~:- Oedema B.B. FIG. 1. Locus and extent of lesions in brain-damaged patients. Maps reconstructed from CT scans (Luzzatti el al., 1979).
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E.G.
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RESULTS
In Table 1 the scores of correct difference-detections on the left (DDL) and on the right side (DDR) of static patterns are shown. The right-left gradient
TABLE 1. STATIC PATTERNS
Mean DDL and DDR Group Control Brain-damaged-
DDL* 3.60 1.37
DDR* 4.10 4.58
(DDR-DDL) was found to differ significantly between the patients and the control group (t (47) = 6.26, P < 0.0001). The data related to dynamic patterns are shown in Table 2, where separate scores for left- and rightward trials are given. From these
TABLE 2. DYNAMIC PATTERNS
Mean DDL and DDR in Left- and Rightward Conditions Group Control Brain-damaged
DDL* Leflw. 2.40 1.58
DDL* Rightw. 3.40 2.47
DDR* Leflw. 3.20 3.10
DDR* Rightw. 2.40 2.16
Maximum scores = 6.00.
scores, the effects of Side, Recency and Direction of the patterns' movement were calculated as shown in Table 3. A 3-variate, one-way analysis of variance (Anderson, 1958) showed that the overall between-groups difference due to these effects was significant (F (3, 45) = 3.338, P = 0.027). Multiple comparisons were therefore carried out in order to test the three effects separately (Roy and Bose, 1953; this method yields theta-points derived from the generalized beta-distribution, which
TABLE 3. DYNAMIC PATTERNS
Effect of Side, Recency and Direction of Movement on the Detection of Differences Group Control Brain-damaged 1 2 3
Side' -0.20 + 1.21
Recency2 + 1.80 + 1.83
Direction of Movement3 +0.20 -0.05
(DDR leftw.+ DDR rightw.)-(DDL leftw. + DDR rightw.). (DDL rightw. + DDR leftw.)-(DDL leftw.+ DDR rightw.). (DDL rightw.+ DDR rightw.)-(DDL leftw.+ DDR leftw.).
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* Maximum scores = 6.00.
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EDOARDO BISIACH AND OTHERS
could here be converted into points of the F-distribution). The effect of Side was thus found to be significantly different in controls and brain-damaged patients (F (3, 45) = 3.097, P — 0.036) whereas the differences concerning the other two effects were far from being significant (F (3, 45) < 1). DISCUSSION
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We begin by making some preliminary remarks with regard to dynamic patterns. Differences on the left halves of these patterns were more apt to be overlooked by our patients than by subjects in the control group: an overall left/right gradient of performance is apparent in the patients, even if in the case of rightward moving patterns this is counteracted by the strong recency effect, which affected equally the performance of both patients and controls. Actually, the patients scored better on the left, rather than the right half of rightward moving patterns (the former being the last half perceived) but it is important to notice that the difference is not as pronounced as in controls. Oculomotor disorders were present in 81.24 per cent of our patients, a finding which is in agreement with Hecaen's (1962) data on the association of these disorders with unilateral neglect. The hypothesis that oculomotor disturbances might somehow have affected the performance of our patients seems to lack validity as the effect of the direction of moving patterns is negligible. This hypothesis is further undermined by the fact that in the three patients who did not show oculomotor disorders the mean Side effect ( + 1.00) was of the same order as that found in the entire group of patients. Taking all this into consideration, it would appear to be reasonably safe to make a further analysis of the experimental results in terms of unilateral neglect. Though the data of dynamic patterns can better develop our argument, we think that even the most obvious phenomena of unilateral neglect as those witnessed in the first part of the experiment would claim the primary explanatory role of a representational disorder. This would, however, require the assumptions that (a) the nervous system cannot conceivably be programmed to gather information without recruiting an inner model of the source thereof, and (b) that any unmonitored failure in performing the programme implies a breakdown of the model itself. To state this in simpler terms, we think that in the cases of patients like ours the loss of sensory information about one side of space could be easily remedied through exploratory activity initiated by the intact neural structures, if all expectations relative to that side of space were not lacking as a result of the lesion. The incorrigibility of this state even by external pressures, which can be observed in most pronounced cases of unilateral neglect, would suggest that the left side of space has not disappeared from consciousness owing to an Amnesie der linken Seite (Zingerle, 1913). On the contrary, we would suggest that in these instances the actual possibility of conceptualizing the existence of a left side is in fact precluded. In any case, a primary disorder of the spatial schema subtending mental representations is selfevident in the second part of the experiment. All spatial features of the patterns
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The same conclusion had been reached with reference to left-sided omissions from verbal descriptions of remembered perspectives (Bisiach and Luzzatti, 1978). Hence it is likely that the same spatial schema is involved in the two instances, even though the source of the processed information is different. Pylyshyn (1973) has warned against possible misuses of the phenomenological concept of 'image' as an explanatory construct in psychological theories. He states that visual representations are 'much closer to being a description of the scene than a picture of it'. None the less, our findings suggest that the spatial attributes of representations cannot be accounted for solely in terms of propositional retrieval: their left side fades in consequence of right hemisphere impairment, so that their spatial schema appears to be mapped across the brain. Non-localizationistic views of conscious brain activity, of which one of the most intriguing up-to-date developments is holographic models (Pribram, 1971, 1972, 1977; Pribram, Nuwer and Baron, 1974), must face the weight of this evidence afforded by unilateral neglect, even though the major manifestations of the latter are so amazingly ephemeral. Finally, the crucial share of the right hemisphere in the structuring of the representational schema in question does not support existing claims which by mistaking consciousness as being the ability to communicate the contents thereof verbally confine it to the left hemisphere of the brain (Eccles, 1976; Popper and Eccles, 1977; Weimer, 1977). On a more general ground, it is not possible in our opinion to accommodate the data in question by interactionistic theories of mind {see Popper and Eccles, 1977). A mind, not co-extensive with part of the brain, would of necessity be endowed with its own invulnerable model of the world if it were to be able to read out from nervous activity and act on it coherently. Accordingly, it would not endorse the
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shown in the first part were in fact simultaneously displayed and invariant throughout the time of each individual exposure. Some of them might fall into the unattended visual field of brain-damaged patients and be neglected. By contrast the same configurations, when appearing behind the slit, were delineated by a narrow, ever-changing section. Instead of a direct, isomorphic (at least in its earliest stages), neural correlate of their entire shape, it is conceivable that under these viewing conditions, a temporally structured pattern of excitation took place in those formations which subserve vision in proximity to the vertical meridian of the visual field. In order to perceive a moving cloud under these conditions it becomes necessary to effect a translation from an objective temporal dimension into a representational spatial one. Our findings suggest that also the left side of this kind of graph drawn in a merely representational space may to some extent fade into unilateral neglect. It is worth emphasizing that under these viewing conditions no inattention to parts of stimuli occurs and that unilateral neglect affects the internal representations of these stimuli manifesting itself in the left side of the reconstructed cloud, irrespective of whether this side refers to its leading or trailing edge. A topological relationship, therefore, seems to link to the neural substrate the spatial schema where these percepts take shape.
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oblivion of one side of the world, even less that of the representational world. On the contrary, it would counteract oblivion by resorting immediately to the surviving neural structures, which would be potentially quite adequate to overcome the defect. This is, in fact, the interactionist's expectation, as expressed by Popper: '. . . the liaison brain is, as it were, almost an object of choice of the selfconscious mind. That is to say, if a certain part of the brain is not available, the self-conscious mind will seek another part as substitute.' (loc. cit., p. 495) which is refuted by the syndrome of unilateral neglect.
SUMMARY .
ACKNOWLEDGEMENT Research supported by CNR Grant CT7701246.
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