Neural Mechanisms of Spatial Neglect
Istituto di Fisiologia Umana, Università degli Studi di Parma, Parma, Italy
Introduction
We have recently advanced a theory of neglect based on the functional properties of the brain areas whose damage produces neglect (Rizzolatti & Berti, 1990). The main points of this theory are as follows:
In this chapter, we will discuss some of the statements presented above and in particular the relation between attention and neglect (outlined in Rizzolatti & Berti, 1990). In addition, we will review some recent clinical observations which show how the representational theory of neglect is heuristically powerful in explaining some intriguing aspects of the syndrome.
Attention and Neglect
An Initial Problem: What Attention Means
Neglect has often been considered a syndrome that is due basically to a disturbance of attention. This idea derives naturally from the observation that patients with neglect ignore (“do not pay attention to”) space contralateral to the brain damage; hence the conclusion that these patients have a disorder of attention. It is obvious that, without a precise terminological specification, this interpretation of neglect is more a tautology than a scientific account of the syndrome. Any theory which wants to explain neglect as an attentional disturbance must, first of all, define attention. To rephrase William James (1890): “No one knows what attention is”, or, at least, there is no obvious agreement on what different authors mean when they use this term. Secondly, the theory must predict which behavioural and cognitive deficits damage to the attentional mechanism (clearly defined) would produce. If these requests are not fulfilled, a theory of neglect as an “attentional” disturbance is devoid of any scientific value.
Early vs Late Selection
William James (1890), pp. 403–404 defined attention as “the taking possession by the mind, in clear and vivid form of one out of what seem several simultaneously possible objects or trains of thought”. From this definition, it is clear that, originally, attention was thought of as a mechanism whose function was the selection for perception of external stimuli or internal states. Once attention is defined as selection, the fundamental theoretical problem is to assess how people select information from the environment and how they deal with irrelevant information.
A major controversy on this issue has been the level at which selection occurs. Early selection theorists maintain that elementary features of the visual world, such as contours and lines, which have the attributes of orientation, contrast, length and width, are represented before attentional selection. If the unattended stimuli fall outside the focus of attention, they are filtered out (Broadbent, 1982; Johnston & Dark, 1982; Treisman & Gelade, 1980). In contrast, late selection theorists claim that attention operates after stimulus identification and therefore the irrelevant aspects of the environment are also fully analysed (e.g. Deutsch & Deutsch, 1963). Although the problem is not solved, data on the so-called “interference effect” (e.g. Stroop, 1935) appear to indicate that some processing of the unattended stimuli is carried out beyond the stage of elementary feature analysis. Furthermore, recent data have shown that stimuli that do not interfere with the subject’s primary task may also produce a negative priming effect, that is a decrease in performance when such stimuli are followed by others somehow related to them (see Allport, Tipper. & Chmiel, 1985; Driver & Tipper, 1989).
Attention as a Facilitatory Mechanism
Another way to view selective attention is to consider it as a mechanism which facilitates the processing of certain stimuli or certain space positions. This view is based on experiments which show that stimulus cueing increases processing efficiency. The paradigm most commonly used to demonstrate this effect is that described by Posner (1980). In this paradigm, reaction times to stimuli presented at cued and uncued positions in the visual field are measured. The difference between them is taken as an index of the detection efficiency of the cued position. Stimuli at cued positions are presented more frequently than stimuli at uncued positions and the subject has to respond regardless of stimulus location.
Two types of cues have been used: symbolic cues and peripheral cues. Symbolic cues are centrally presented symbols (arrows, numbers) which indicate the most likely stimulus position. The subject has to interpret them in order to allocate attention to the correct position. Peripheral cues are visual stimuli presented in the correspondence of the location of the imperative stimulus. Peripheral stimuli are thought to attract the subject’s attention automatically (e.g. Jonides, 1981). Both symbolic and peripheral cues produce a clear advantage of the cued positions with respect to the uncued ones. These data have been interpreted as evidence that selective attention acts as a mechanism which gives salience to the cued stimuli, rather than as a filter eliminating, partially or totally, irrelevant information. An analogy has been proposed in which the beam of a spotlight illuminates only a part of the space at any one time (Posner, 1980; Remington & Pierce, 1984; see also Umiltà, 1988). In accordance with this metaphor, attention is considered as unitary and it is postulated that in the brain there is a specific, anotomically definable circuit (see Mesulam, 1981; Posner, Walker, Friedrich, & Rafal, 1984) which controls attention. The activity of this circuit can be modulated endogenously (cognitive cues) or externally (peripheral cues). This assumption is not a necessary consequence of empirical data. It is based in part on introspection, but mostly derives from the notion, very popular among cognitive psychologists, that a central processing system, similar to that at the core of digital computers, should exist in the brain (see, e.g. Shallice, 1988). As will be shown later, this aspect of the theory is questionable. Evidence against it will be presented in the next section.
Attention as Selection for Action
A rather different perspective on attentional functions than the traditional ones has been advanced by Allport (1987; 1989). According to his theory, the fundamental purpose of attention is the choice of a specific action directed towards a given object, rather than the selection of a single stimulus among the many that are present in the environment. The senses are considered capable of registering many different stimuli simultaneously. It is the effector system, which is typically limited in its capacity, that carries out one single action at a time. The need for a mechanism for coupling and decoupling perceptual and motor processes is the basis of the attentional mechanism. This mechanism can be triggered externally by particular stimulus conditions or by internally generated states.
An emphasis on the mechanisms responsible for the selection of action is also found in the pre-motor theory of attention (Rizzolatti, 1983; Rizzolatti & Camarda, 1987; Rizzolatti, Riggio, Dascola, & Umiltà, 1987). This theory differs from the filtering or spotlight theories of attention in two ways:
Evidence in favour of the first point comes from a wide range of data, on monkeys as well as humans (see references in Rizzolatti & Gallese, 1988), that indicate a close relationship between motor organisation and attentional behaviour. The strongest evidence is probably the demonstration of dissociations between the capacity of processing stimuli presented in different sectors of space following lesions of different brain centres (Rizzolatti, Gentilucci, & Matelli, 1985). The dissociations are hardly explained by a single attentional centre. Arguments in favour of the second point will be discussed at the end of this chapter.
Can Attentional Theories Explain Neglect?
Even if the precise meaning of “attention” is specified, the question arises as to what is meant when neglect is explained by an attentional deficit. Does it mean that an early or late filtering process has been impaired by the brain lesion? Or that some kind of spotlight mechanism is not working properly? Or that patients are unable to combine the appropriate motor behaviour to the selected stimulus? Or, finally, that some of their pre-motor circuits have been damaged?
As far as the filtering theories are concerned, it appears logical to expect that if some kind of filter is damaged, the patient should have difficulties in selecting the relevant stimuli in the space contralateral to the lesion. The patient will have confused perception due to difficulties in parsing the contralateral field in a clearly defined percept. Contrary to this prediction, patients with neglect ignore the contralesional space, without behaving as if they were perceptually confused due to a non-monitored selection of contralesional stimuli. It would therefore appear to be unrealistic to view neglect as a problem of information filtering.
Allport’s (1989) interpretation of attention, although conceptually different from the filtering hypotheses and theoretically very appealing, encounters the same difficulties as the filtering hypotheses in explaining neglect. Indeed, incapacity of coupling and decoupling percepts and motor actions, which are at the core of Allport’s theory, should produce incoherent motor behaviour with the performance of apparently meaningless acts.
The spotlight theory proposes that attention “is a limited capacity system that might be identified with conscious awareness” (Posner, 1982). Attention, therefore, is the mechanism that gives salience to different stimuli and allows individuals to become aware of their presence. Thus, if neglect were a disorder of attention in this sense of the term, one should expect patients with neglect to have a complete lack of awareness of any type of stimuli and in any part of space. However, patients’ symptomatology does not correspond to these predictions. First, the symptomatology is more severe in the field contralateral to the lesion, whereas it would be bilateral if there was one centre for directing attention. Secondly, both in the monkey and man, several dissociations have been described as far as visual stimuli, space sectors and types of response are concerned. All these dissociations cannot be accounted for by a single attentional centre. Thirdly, as reviewed by Rizzolatti and Gallese (1988), the anatomical connections of the areas whose lesions produce neglect indicate the presence of several independent circuits rather than the presence of only one circuit selectively responsible for attention. Finally, data on the anatomy of the attentional system, gathered from PET studies, provide clear evidence against the idea of a single attentional centre (Corbetta et al., 1990; Posner, Petersen, Fox, & Raichle, 1988). Areas related to different types of attention have been described in the occipital lobe, the frontal lobe and the cingulate cortex. To date, the parietal areas have been found to be little activated, if at all. While this last observation is most likely due to the materials and tasks employed, there is no doubt that the notion of a single attentional centre or circuit for attention in the cortex has been “falsified” by PET studies.
The demonstration of a multiplicity of areas involved in attention is consistent with the main tenet of the pre-motor theory that attention is not a supramodal function, as claimed by most cognitive psychologists, but a function mediated by several independent circuits (see Rizzolatti & Gallese, 1988). This claim was based essentially on neurophysiological studies in monkeys which indicated that there is no anatomical centre that has a privileged connection with attention. These studies demonstrated that even spatial attention is not a unitary function, but consists of several separate mechanisms mediated by anatomically and functionally independent circuits. There is, however, one neglect finding which appears to be difficult to explain using the pre-motor theory of attention. Lesions which destroy only one sensori-motor circuit often produce neglect for all kinds of stimuli coming from the affected space sector (Rizzolatti, Matelli, & Paresi, 1983). This deficit is observed despite the presence of other circuits able to process the same stimuli in parallel. If attention is a mechanism which facilitates the processing of information, but which is not necessarily required for it, the prediction of the pre-motor theory, in the case of limited lesions, is extinction and not neglect. If, on the other hand, attention is a prerequisite for conscious awareness, the pre-motor theory appears able to accommodate the findings. One wonders, however, whether the term attention is really the most appropriate in this case and whether there is no other term more adequate to describe the phenomenon. Considering the anatomical/physiological organisation of the areas whose lesions produce neglect, the term representation, in our opinion, reflects much better the fundamental mechanism which is destroyed in neglect. We will return to this point in the second part of this chapter.
While the pre-motor theory of neglect does not seem able to explain without further assumptions the fully fledged symptoms of neglect, it can provide an explanation of the fact that patients with neglect may show a gradient of preference for stimuli in the normal field with a better performance for those most ipsilesional (De Renzi, Gentilini, Faglioni, & Barbieri, 1989; Kinsbourne, 1987; Làdavas, Petronio, & Umiltá, 1990; sec also Chapters 3 and 9, this volume). It is well established that motor organisation is based on a series of reciprocal inhibitions between competing programmes. This is found at the simple level of motor organisation, as for example in the spinal cord (Sherrington, 1906), but it also observed at higher neural levels. The oculomotor and vestibular systems are classical examples of this type of organisation. If, as the pre-motor theory maintains, there is a close link between motor programming and attention (stimulus processing facilitation), unilateral damage should release the motor programmes in the intact side of the brain from the control usually exerted by the opposite side of the brain, thus favouring the motor and attentional operations in the ipsilateral (normal) visual space. The existence of this kind of interaction between operations in the two visual fields was demonstrated by Sprague (1966). He showed that a stable contralateral hemineglect occurs in cats after large parieto-occipital cortical lesions. A subsequent lesion, either of the ipsilateral superior colliculus or the intertectal commissure, markedly improves the symptomatology, with recovery of the responses in the previously neglected field. The most likely interpretation of this finding is that, after the first lesion, the visuo-motor circuits for ipsilesional orienting responses are liberated from the control of the competing contralateral programmes. The consequence is a prevalence of visuo-motor orienting behaviour towards ipsilesional space and an inhibition of the residual contralateral circuits. The second lesion, by severing the link between competing programmes, restores the residual circuits responsible for head and eye movements towards the previously neglected side and, consequently, restores also the capacity to orient attention towards this side.
In conclusion, this survey of the definitions and theories of attention shows that none of them appears to be sufficient to explain all aspects of the neglect syndrome. In the next section, we will provide evidence that at the core of the disturbance is a deficit of space representation.
Representation and Neglect
The definition of neglect as a representational deficit has been revived in the neurological literature by Bisiach and co-workers (Bisiach & Berti, 1987; Bisiach & Luzzatti, 1978; Bisiach, Luzzatti, & Perani, 1979). They showed that neglect can be demonstrated in conditions in which no stimuli are presented to patients who are asked to perform mental operations involving imaging. The most striking result was that their patients were able to reconstruct visually only the ipsilateral half of the requested image. These studies aroused new interest in neglect and offered an alternative to the attentional explanations. However, Bisiach and co-workers’ experiment may have an alternative explanation. One can postulate that, although the spatial representation is intact, neglect patients have a lesion of the attentional mechanism which facilitates the ipsilesional representation. We have already discussed the difficulty that attentional interpretations encounter in explaining neglect. However, the possibility that some attentional mechanisms may have a role to play in the phenomenon described by Bisiach and co-workers cannot be ruled out completely (see below).
Neural Representation Theory of Neglect
The neural representation theory of neglect makes two claims about how space is represented in normal subjects: (1) space is represented in several brain centres and, under normal circumstances, the joint activity of these centres is responsible for conscious space awareness; (2) the centres responsible for conscious space awareness code space using viewer-centred co-ordinates. Damage to areas where space is coded in these co-ordinates leads to neglect, while damage to areas where space is coded in retinotopic co-ordinates leads to hemianopia.
Neurophysiological evidence in favour of the first claim is compelling and will not be reviewed here (see Rizzolatti & Gallese, 1988). The second claim is more controversial and requires specification. It can be formulated in two forms. In one form, it says that space is explicitly coded by neurons which have spatial receptive fields. The activity of these neurons signal the location of an object in the space relative to the viewer, independently of eye position. In another form, it postulates that viewer-centred space derives from computation due to neurons whose receptive field is coded in retinotopical co-ordinates.
Empirical evidence in favour of neurons with a spatial viewer-centred receptive field (explicitly spatial, ES) is very strong for the peripersonal space. In monkey area 6, many neurons respond to stimuli presented in particular body-related space sectors, regardless of eye position (Fogassi et al., 1992; Gentilucci, Scandolara, Pigarev, & Rizzolatti, 1983; Gentilucci et al., 1988; Rizzolatti & Gentilucci, 1988). These neurons have bimodal (tactile and visual) fields, with the visual field anchored to the tactile one. A similar organisation is present in area 7b, a parietal area strictly linked to inferior area 6 (Hyvarinen, 1982). Bimodal ES neurons have also been described in area 6 of the cat (Pigarev & Rodionova, 1986).
The existence of spatial neurons is not so obvious in the case of monkey parietal areas involved in the extrapersonal space representation. Studies of area 7a and of an area adjacent to it (LIP) have shown that in these areas several neurons have retinotopically organised receptive fields gated by eye position (Andersen, Essik, & Siegel, 1985, 1987; Sakata, Shibutani, & Kawano, 1980). This finding and the apparent lack of viewer-centred space neurons in the same areas led Andersen et al. (1990) to conclude that viewer-centred space representation derives from the activity of eye-modulated retinotopical neurons. A computational model showing that position in the space could be computed by units with properties similar to those described in area 7a appeared to confirm this point of view (Zipser & Andersen, 1988).
Recent experiments, however, indicate that neurons with a viewer-centred receptive field are not limited to areas related to peripersonal space. Pigarev and Rodionova (1988) demonstrated that in the cat, ES neurons are abundant in the parietal lobe. These neurons are unimodal and respond also to far stimuli. Very recently, ES neurons have also been demonstrated in area V6 of the monkey (Battaglini, Fattori, Galletti, & Zeki, 1990). Thus, although at the present time one cannot rule out completely the hypothesis that the space representation for extrapersonal space might derive from eye modulation of retinotopically organised neurons, this hypothesis appears to be weakened by these new experimental data. It is possible that visual neurons modulated by eye position are an intermediate step between retinotopical maps and explicit spatial representations. Congruent with this point of view are the observations that eye-modulated visual neurons are also present in the retinotopically organised prestriate areas of the occipital lobe (Galletti & Battaglini, 1989) and in the pulvinar (Robinson, McClurkin, & Kertzman, 1990).
Object Analysis and Space
There is general agreement that space and object perception are mediated by the activity of two separate series of cortical areas and that, broadly speaking, the temporal lobe is mostly involved in object perception, whereas the parietal lobe is mostly involved in space perception (Ungerleider & Mishkin, 1982). Object analysis, however, entails two different sets of operations. One concerns object reconstruction from its elementary features and its recognition despite its possible different locations in space and different angles of view. These operations are most likely carried out in the inferotemporal lobe (Gross, 1973). The second set of operations concerns the description of objects in spatial terms. This description requires, in turn, different types of operations. The first is the location of objects with respect to the viewer. The second is the matching of the viewer-centred space with the centre of the object (viewer-centred object representation). An overt example of this matching is represented by head movements which align the head vertical axis with the object even when the object is misplaced with respect to it, even a few degrees. We postulate that a similar object-viewer matching also occurs covertly. Both the location of objects in space and the object-viewer alignment, which are spatial in their essence, are most likely performed in the parietal lobe. The third operation is the extraction of the intrinsic object properties (see Jeannerod, 1988; Arbib, 1981). Neurons coding the intrinsic properties of the object (size, shape, orientation) have been described in inferior parietal lobe (Taira et al., 1991) and in the premotor areas connected with it (Rizzolatti et al., 1988). Thus the involvement of the dorsal visual stream of information in object analysis is not a mere supposition but a well-proved fact (see also Goodale & Milner, 1992).
Predictions of the Neural Representation Theory
Once the two claims of neural representation theory are accepted, two main predictions may be advanced as far as the neglect symptoms are concerned: (1) the presence of dissociations between various representational domains (personal, peripersonal and extrapersonal space; space and object representation); and (2) the implicit processing of information within the neglected space. In the next paragraph, we will examine how clinical observations fit with these predictions. Particular emphasis will be given to those data that were not reviewed in our recent article on neglect (Rizzolatti & Berti, 1990).
Dissociations. A dissociation between personal and extrapersonal neglect in man was first described by Bisiach, Perani, Vallar and Berti (1986) in patients with unilateral brain damage. The patients undertook two tasks aimed at assessing unilateral neglect in personal and extrapersonal space. The authors found that personal neglect was much less frequent than extrapersonal neglect. Extrapersonal neglect could, therefore, be seen in the absence of personal neglect. In addition, they also found a patient who showed a severe neglect for personal space without any convincing symptoms of extrapersonal neglect. A similar case has recently been observed by Guariglia and Antonucci (1992). Their patient, whom they studied using a battery of tests specifically devised to assess personal neglect, showed a severe personal neglect while no deficits of any kind were present in extrapersonal space.
Recently, Shelton, Bowers and Heilman (1990) examined the behaviour of normal subjects and of a neglect patient when bisecting lines presented radially (pointing away from the subject) in peripersonal space. The lines were positioned adjacent to the body surface (near peripersonal space), with the line midpoint 30 cm from the body (middle peripersonal space) or 60 cm from it (far peripersonal space). The most striking result was that the patient consistently made a misplacement error towards the near end of the line. Furthermore, the error was small in the near peripersonal space, whereas it was large in the far peripersonal space. The authors interpreted these data as evidence for a subdivision of space representation in sectors (see also Rizzolatti et al., 1983) and as an indication that each of these sectors can be impaired separately.
An opposite dissociation has been observed by Halligan and Marshall (1991). They found a patient who showed a classical extrapersonal neglect when tested on line bisection and other standard tests for the neglect syndrome. However, his deficits were minimal or absent when he had to perform motor action in far space. When requested to bisect a line positioned outside his reaching distance, either with a light pointer or by throwing darts, he performed in the normal range.
Another interesting space dissociation, which was recently reported, is the presence of neglect concerning the vertical dimension—altitudinal neglect (Rapcsak, Cimino, & Heilman, 1988). The deficit is found most frequently in the lower part of the visual space. Halligan and Marshall (1989) found lower field neglect in 18 of 23 patients with neglect, while only 2 presented neglect for the top half of the display, and 3 made the same number of errors in each half.
Deficits along the vertical dimension have previously been described following mesencephalic lesions both in animals and man. Matelli, Olivieri, Saccani & Rizzolatti (1983) found two distinct neglect syndromes in the cat that depended on the mesencephalic commissures that had been cut. The first syndrome occurred after a complete section of the commissure and involved the upper space as well as head and eye movements directed towards this space sector. The second syndrome appeared following the lesion of the posterior commissure and the rostral part of the intertectal commissure. In this case, the disturbances concerned the lower space as well as eye and head movements that were directed downwards. Deficits along the vertical plane were also demonstrated in patients affected by progressive supranuclear palsy (Posner, Cohen, & Rafal, 1982; Rafal & Grimm, 1981). Also in these patients, there was a congruence between the altitudinal deficit and the deficit of eye movements.
A mechanism similar to that described for mesencephalic neglect may be postulated for parietal patients with altitudinal neglect. It is likely that in this case also, circuits are lesioned that are responsible for the representation of a given space sector and for operation on it. The large prevalence of lower space deficits is probably due to the fact that this is the space sector in which manipulations mostly occur (see Previc, 1990). Considering the importance of the parietal lobe for operation in the peripersonal space (see Mountcastle, 1976), it is very likely that lower visual space is particularly richly represented in this part of the brain. Lesions of the parietal lobe, therefore, are more likely to hit the representation of the lower part of the visual space than the upper part.
Recently, another dichotomy has been pointed out regarding neglect. Gainotti, D’Erme, Monteleone & Silveri (1986) noticed that, in copying a complex drawing, a neglect patient ignored the left part of each object depicted in the model, instead of neglecting, as most patients do, the left part of it. Driver & Halligan (1991) observed a patient who behaved in a similar manner to that of Gainotti and co-workers’ patient when copying models and during a particular version of the cancellation task. Moreover, they found that the patient had a strong tendency to neglect the left side of stimuli even when they were rotated and the left part of the stimulus was on the right side of the display. These findings were interpreted as the demonstration that some patients have selective difficulties with spatial representations of the objects. Note, however, that the reported deficit implies a distinction between left and right, i.e. the sides of the objects as referred to the viewer. The deficit is therefore a special case of a viewer-centred representational deficit rather than an object-centred defect. In a true object-centred representational deficit, a certain part of an object should be constantly neglected, regardless of its position with respect to the viewer. For example, in the case of a rabbit, a patient should always ignore its head or tail independently of where the rabbit is looking. As far as we know, no such cases have been described (see Farah et al., 1990, for a discussion of this point) and, according to our definition of neglect, such cases (if found) would not belong to the domain of neglect.
An explanation in terms of viewer-centred object representation can also be suggested for the findings of Caramazza and Hillis (1990). They described patient N.G. who made reading and spelling errors on the right half of words. The striking feature was that N.G. showed the same pattern of errors irrespective of the spatial arrangement of the stimuli. Since it was the part of the word which was on the right in horizontal normal word presentation which was neglected, even when the word was presented vertically or mirror-reversed, this case suggests that the representation of words is spatially encoded along a horizontal axis referred to the viewer. When the word was presented in a non-canonical way, the subject had to adjust it, so that his subjective midline coincided with the word midline. As mentioned above, this adjustment occurs overtly in the case of object presentation and represents the ideal relation between viewer and object in order to act upon it (for a discussion of neglect dyslexia, see Chapter 11 this volume).
A further case of the viewer-centred object representational deficit has been described by Young, de Haan, Newcombe, and Hay (1990). Their patient showed left neglect only for physiognomic material and no other sign of sensory or representational disorders. Although these authors suggest that the deficit in this case could be due to a disorder of a “face-specific” attentional mechanism, we believe that a representational interpretation explains this finding much better. Indeed, the assumptions of a specific circuit for “face attention” is arbitrary, whereas there is no doubt that there are neural centres specifically related to face representation (Perrett, Mistlm, & Harries, 1989).
Implicit Processing. The second prediction of our theory is that, given the multiplicity of circuits involved in space representation, neglect patients may show implicit processing of the information coming from the space sector contralateral to the lesion. Volpe, Le Doux and Gazzaniga (1979) showed that patients with right parietal lesion and clinical evidence of extinction were able to name objects when they were presented singly in either field, but denied seeing the left-side stimuli when two visual objects were presented simultaneously to the right and left of the fixation point. Despite the fact that the patients were unable to name the left object in the simultaneous stimuli presentation, they were still able to make a same-different judgement when forced to do so by the examiner. The authors interpret this finding as evidence for the existence of implicit knowledge of the stimuli, even when the patients were unable to name them or were unaware of their presence.
A capacity for processing information in an implicit way has been described by Marshall and Halligan (1988) in a patient with a severe neglect. This patient was repeatedly presented with two drawings of a house, one above the other. The two houses were identical on the right side but were different on the left side. The patient denied any difference between the pairs of houses even when one of them was seen to be burning. None the less, when forced to choose the one in which she would prefer to live, she always chose the one that was not burning.
Recently, Bisiach and Rusconi (1990) replicated Marshall and Halligan’s experiment in four patients with neglect, using different kinds of stimuli. They also found that the neglected side of the figure influenced the patients’ responses. This influence, however, varied from one patient to another, and was not necessarily related to the meaning of the features which should determine the logically correct choice. For example, two of their patients consistently preferred the burning house. This suggests that it is not necessarily the meaning but sometimes also the mere presence of some low-level sensory factors that may determine choice.
However, a demonstration that in some cases high-level processing can be responsible for the patients’ judgement of material presented in the neglected field has been provided by a study on a patient with extinction (Berti et al., 1992). The authors replicated Volpe and co-workers’ study using pairs of pictures of identical objects taken from the same or different viewpoints, pairs of different examplars of the same category of objects and pairs of different objects. Patient E.M. could not name left-sided stimuli. However, she was still able to make correct same-different judgements, both in the same and different trials, even when the two objects were physically dissimilar but belonged to the same category. This study showed that patients can make categorical judgements on the objects presented in the extinguishing field even when they are not aware of its identity.
Even more compelling for the issue of implicit processing in neglect patients is a recent study by Berti and Rizzolatti (1992). They demonstrated that in patients with severe neglect, a prime stimulus presented to the neglected visual field can facilitate the responses to target stimuli presented to the normal field. This effect was present when the priming stimulus was physically identical to the target and, most importantly, also when the prime and the target were physically different but belonged to the same category of objects. Note that five out of the seven neglect patients in this study appeared to be hemianopic either on perimetry testing or on confrontation and did not report the presence of any left stimulus in the preliminary part of the experiment. Similar results have been obtained also by McGlinchey-Berroth et al. (in press).
Conclusion
It is a classical notion of neurology that after brain damage two types of symptoms can emerge, negative symptoms and positive symptoms (Jackson 1881). Negative symptoms are the direct consequence of the lesion; positive symptoms derive from the release of centres connected with the damaged brain part. Thus, as an example, in the case of spastic paralysis, the negative symptom consists of the inability to perform voluntary movements, whereas the positive manifestation is the increase in muscular tone. We propose a similar interpretation for neglect symptoms. According to this interpretation, the inability to consciously process information coming from the neglected field, represents the neglect negative symptoms. It is due to a lesion of some, or all, of the space representations as defined in the previous paragraphs. The positive symptoms manifest themselves essentially in the shift of processing capacity towards the side ipsilateral to the lesion (for a comprehensive discussion of this symptom, see Chapters 3 and 9, this volume). As a consequence, the right-most stimuli are perceived better and responded to faster. Positive symptoms may aggravate the representational deficit in a similar way that spasticity aggravates paralysis. They are not, however, the primary cause of neglect.
This interpretation of neglect in terms of positive and negative symptoms fits well with some interesting recent neurological observations. Rubens (1985) showed that a caloric stimulation of the vestibular system, which produces a shift of the eyes towards the neglected side, can improve the neglect symptomatology. This observation was confirmed by Cappa, Sterzi, Vallar and Bisiach (1987), who demonstrated that vestibular stimulation can also improve other representational deficits like anosognosia. The same effect was shown for a productive symptom like somatoparaphrenia (Bisiach & Rusconi, 1991). The stimulation of the vestibular system in the above-cited experiments has, as its primary consequence, an activation of the vestibulo-motor circuits of the damaged side of the brain, which, within limits, compensates for the imbalance between the motor circuits of the two sides of the brain. In turn, according to the pre-motor theory of attention, this compensation improves the attentional mechanisms linked to them. From this, two consequences derive. First, moving attention towards the neglected side decreases the severity of the positive symptoms related to the right shift of processing capacity. Secondly, and most importantly, the activation on the ipsilesional side of the spared centres responsible for space representation determines the restoration of the awareness of the space contralateral to the lesion. It is important to note that an improvement in attention alone cannot explain recovery from anosognosia. It is well known that anosognosic patients often pay a continuous, almost pathological attention to their affected limbs, still continuing to deny the neurological symptoms (see Bisiach, Meregalli, & Berti, 1990). Thus, if vestibular activation only acts through a selective attentional mechanism, one should expect no improvement in the anosognosic symptoms. In contrast, if vestibular activation restores, through activation of the residual circuits, the personal and extrapersonal spatial representations, such improvement can easily be predicted.
Another example of the usefulness of the subdivision of the neglect syndrome into positive and negative symptoms is represented by some data reported by Doricchi, Guariglia, Paolucci and Pizzamiglio (1990). They studied groups of patients with left-sided brain lesions, right-sided brain lesions without neglect and right-sided brain lesions with neglect. All three groups showed a reduction in rapid eye movements towards the contralesional side during paradoxical sleep. However, this reduction was much stronger in the neglect group than in the other two groups. This observation confirms the strict link between the representational deficit of neglect and motor programming. In addition, Doricchi et al. (1990) found that neglect patients who showed significant improvement after a rehabilitation programme continued to present an almost complete lack of contralesional eye movements during paradoxical sleep. The fact that during wakefulness—that is, in a situation in which attentional resources can be called in—there was an improvement, whereas during sleep the basic deficit remained unchanged, suggests that attention is not the primary mechanism responsible for neglect. On the contrary, once it is accepted that the lack of eye movements is an indirect measure of the primary disorder, the findings of Doricchi et al. (1990) fit well with the representational theory. Note that according to this theory, although the representational deficit is primary, its severity can be influenced by attentional pre-motor circuits.
Acknowledgements
We would like to thank Edoardo Bisiach for his suggestions and comments. This work was supported by grants from CNR and MPI to G.R.
Allport, A (1987). Selection for action: Some behavioural and neurophysiological considerations of attention and action. In H. Heuer & A.F. Saunders (Eds), Perspectives on perception and action. Hillsdale, NJ: Lawrence Erlbaum Associates Inc.
Allport, A. (1989). Visual attention. In M.I. Posner (Ed.), Foundation of cognitive science. Cambridge, MA: MIT Press.
Allport, D.A., Tipper, S.P., & Chmiel, N.R.J. (1985). Perceptual integration and postcatego-rical filtering. In M.I. Posner & O.M. Marin (Eds), Attention and performance XI. Hillsdale, NJ: Lawrence Erlbaum Associates Inc.
Andersen, R.A., Bracewell, R.M., Barash, S., Gnadt, J.W., & Fogassi, L. (1990). Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of Macaque. Journal of Neuroscience, 10, 1176–1196.
Andersen, R.A., Essik, G.K. & Siegel, R.M. (1985). The encoding of spatial location by posterior parietal neurons. Science, 230, 456–458.
Andersen, R.A., Essick, G.K., & Siegal, R.M. (1987). Neurons of area 7 activated by both visual stimuli and oculomotor behaviour. Experimental Brain Research, 67, 316–322.
Arbib, M.A. (1981). Perceptual structures and distributed motor control. In V.B. Brooks (Ed.), Handbook of physiology: The nervous system. II Motor Control. Washington, DC: American Physiological Society.
Battaglini, P.P., Fattori, P., Galletti, C., & Zeki, S. (1990). The physiology of area V6 in the awake, behaving monkey. Journal of Physiology, 423.
Berti, A., Allport, A., Driver, J., Denies, Z., Oxbury, J., & Oxbury, S (1992). Levels of processing for visual stimuli in an “extinguished” field. Neuropsychologiu, 30, 403–415.
Berti, A. & Rizzolatti, G. (1992). Visual processing without awareness: Evidence from unilateral neglect. Journal of Cognitive Neuroscience, 4, 345–351.
Bisiach, E. & Berti, A. (1987). Dyschirìa: An attempt at its systemic explanation. In M. Jeannerod (Ed.), Neurophysiological and neuropsychological aspects of spatial neglect. Amsterdam: North-Holland.
Bisiach, E. & Luzzatti, C. (1978). Unilateral neglect of representational space. Cortex, 14, 129–133.
Bisiach, E., Luzzatti, C., & Perani, D. (1979). Unilateral neglect, representational schema and consciousness. Brain, 102, 609–618.
Bisiach, E., Meregalli, S., & Berti, A. (1990). Mechanisms of production control and belief fixation in human visuospatial processing: Clinical evidence from unilateral neglect and misrepresentation. In M.L. Commons, R.J. Herrnstein, S.M. Kosslyn, & D.B. Mumford (Eds), Quantitative analyses of behavior, Vol. IX. Hillsdale, NJ: Lawrence Erlbaum Associates Inc.
Bisiach, E., Perani, D., Vallar, G., & Berti, A. (1986). Unilateral neglect: Personal and extrapersonal. Neuropsychologia, 24, 759–767.
Bisiach, E. & Rusconi, M.L. (1990). Break-down of perceptual awareness in unilateral neglect. Cortex, 26, 643–649.
Broadbent, D.E. (1982). Task combination and selective intake of information. Acta Psychologica, 50, 253–290.
Cappa, S., Sterzi, R., Vallar, G., & Bisiach, E. (1987). Remission of hemineglect during vestibular stimulation. Neuropsychologia, 25, 775–782.
Caramazza, A. & Hillis, A.E. (1990). Spatial representation of words in the brain implied by studies of a unilateral neglect patient. Nature, 346, 267–269.
Corbetta, M., Miezin, F.M., Dobmeyer, S., Shulman, G.L., & Petersen, S.E. (1990). Attentional modulation of neural processing of shape, color, and velocity in humans. Science, 248, 1556–1559.
De Renzi, E., Gentilini, M., Faglioni, P., & Barbieri, C. (1989). Attentional shift towards the rightmost stimuli in patients with left visual neglect. Cortex, 25. 231–237.
Deutsh, J.A. & Deutsh, D. (1963). Attention: Some theoretical considerations. Psychological Review, 87, 272–300.
Doricchi, F., Guariglia, C., Paolucci, S., & Pizzamiglio, L. (1990). Severe reduction of leftwards REMs in patients with left unilateral hemiinattention. In J. Home (Ed), Sleep 90. Bochum: Pontenagel Press.
Driver, J. & Halligan, P. (1991). Can visual neglect operate in object centered coordinates? An affirmative single-case study. Cognitive Neuropsychology, 8, 475–496.
Driver, J. & Tipper, ST. (1989). On the nonselectivity of “selective” seeing: Contrast between interference and priming in selective attention. Journal of Experimental Psychology: Human Perception and Performance, 15, 304–314.
Farah, M.J., Brunn, L.L., Wong, A.B., Wallace, M.A. & Carpenter, P.A. (1990). Frames of reference for allocating attention to space: Evidence from neglect syndrome. Neuropsycho-logia, 28, 335–347.
Fogassi, L., Gallese, V., di Pellegrino, G., Fadiga, L., Gentilucci, M., Luppino, G., Matelli, M., Pedotti, A., & Rizzolatti, G. (1992). Space coding by premotor cortex. Experimental Brain Research, 89, 686–690.
Gainotti, G., D’Erme, P., Monteleone, D., & Silveri. M.C. (1986). Mechanisms of unilateral spatial neglect in relation to laterality of cerebral lesions. Brain, 109, 599–612.
Galletti, C. & Battaglini, P.P. (1986). Gaze-dependent visual neurons in area V3A of monkey prestriate cortex. Journal of Neuroscience, 9, 1112–1125.
Gentilucci, M., Fogassi, L., Luppino, G., Matelli, M., Camarda, R., & Rizzolatti, G. (1988). Functional organization of inferior area 6 in the macaque monkey. 1. Soma-totopy and control of proximal movements. Experimental Brain Research, 71, 475–490.
Gentilucci, M., Scandolara, C., Pigarev, I.N., & Rizzolatti, G. (1983). Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye-position. Experimental Brain Research, 50, 464–468.
Goodale, M.A. & Milner, A.D. (1992). Separate visual pathways for perception and action. Trends in Neuroscience, 15, 20–25.
Gross, C.G. (1973). Visual functions of inferotemporal cortex. In R. Jung (Ed.), Handbook of sensory physiology, Vol. VI1/3. Berlin: Springer-Verlag.
Guariglia, C. & Antonucci, G. (1992). Personal and extrapersonal space: A case of neglect dissociation. Neuropsychologia, 30, 1001–1009.
Halligan, P.W. & Marshall, J.C. (1989). Is neglect (only) lateral? A quadrant analysis of line cancellation. Journal of Clinical and Experimental Neuropsychology, 11, 793–798.
Halligan, P.W. & Marshall, J.C. (1991). Left neglect for near but not far space in man. Nature, 350, 498–500.
Hyvarinen, J. (1982). Posterior parietal lobe of the primate brain. Physiological Review, 62, 1060–1129.
Jackson, J.H. (1881). Remarks on dissolutions of the nervous system as exemplified by certain post-epileptic conditions. In J. Taylor (Ed.), 1958, Selected writings of John Hughlings Jackson, Vol. 2, pp. 12–16. New York: Basic Books.
James, W. (1890). The principles of psychology. New York: Holt.
Jeannerod, M. (1988). The neural and behavioural organization of goal-directed movements. Oxford: Oxford University Press.
Johnston, W.A. & Dark, V.J. (1982). In defense of intraperceptual theories of attention. Journal of Experimental Psychology: Human Perception and Performance, 10, 640–654.
Jonides, J. (1981). Voluntary versus automatic control over the mind’s eye’s movement. InJ.B. Long & A.D. Baddeley (Eds), Attention and performance IX. Hillsdale. NJ: Lawrence Erlbaum Associates Inc.
Kinsbourne, M. (1987). Mechanisms of unilateral neglect. In M. Jeannerod (Ed.). Neurophy-siological and neuropsychological aspects of spatial neglect. Amsterdam: North-Holland.
Làdavas, E., Petronio, A. & Umiltà, C. (1990). The deployment of attention in the intact field of hemineglect patients. Cortex, 26, 307–317.
Marshall, J.C. & Halligan, P.W. (1988). Blindsight and insight in visuospatial neglect. Nature. 336, 766–767.
Matelli. M., Olivieri, M.F., Saccani. A., & Rizzolatti, G. (1983). Upper visual space neglect and motor deficit after section of the midbrain commissures in the cat. Behavioral Brain Research, 10, 263–285.
McGlinchey-Berroth, R., Milberg, W.P., Verfaellie, M„ Alexander, M„ & Kilduff, P.T. (in press). Semantic processing in the neglected field: Evidence from a lexical decision task. Cognitive Neuropsychology.
Mesulam, A.A. (1981). A cortical network for directed attention and unilateral neglect. Annals of Neurology, 10, 309–325.
Mountcastle, V.B. (1976). The world around us: Neural command functions for selective attention. Neuroscience Research Program Bulletin, 14, 147.
Perrett, D.I., Mistlin, A.J., & Harries, M.H. (1989). Seeing faces: The representation of facial information in temporal cortex. In J.J. Kulikowski, C.M. Dickinson, & I.J. Murray (Eds), Seeing contour and colour. Oxford: Pergamon Press.
Pigarev, I.N. & Rodionova, E.I. (1986). Neurons with visual receptive fields independent of eye-position in the caudal part of the ventral bank of cat cruciate sulcus. Neurophysiology (Kiev), 18, 800–804.
Pigarev, I.N. & Rodionova, E.I. (1988). Neurons with visual receptive fields independent of the position of eyes in cat parietal cortex. Sensory System, 2, 245–255 (in Russian).
Posner, M.I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology, 32, 3–25.
Posner, M.I. (1982). Cumulative development of attentional theory. American Psychologist, 37, 168–179.
Posner. M.I., Cohen, Y., & Rafal, R.D. (1982). Neural system control of spatial orienting, Philos. Trans. R. Soc. London ser. B. 298, 187–198.
Posner, M.I., Petersen. S.E., Fox, P.T., & Raichle, M.E. (1988). Localization of cognitive operations in the human brain. Science, 240, 1627–1631.
Posner, M.I., Walker, J.A., Friedrich, F.J., & Rafal. R.D. (1984). Effects of parietal injury on covert orienting of attention. Journal of Neuroscience, 4, 1863–1874.
Previc, F.H. (1990). Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications. Behavioral and Brain Sciences, 13, 519–575.
Rafal, R.D. & Grimm, R.J. (1981). Progressive supranuclear palsy: Functional analysis of the response to methysergide and anti-Parkinson agents. Neurology, 31, 1507–1518.
Rapcsak, S.Z., Cimino, C., & Heilman, K.M. (1988). Altitudinal neglect. Neurology, 38, 277–281.
Remington, R.W. & Pierce, L. (1984). Moving attention: Evidence from time invariant shifts of visual selective attention. Perception and Psychophysics. 35, 393–399.
Rizzolatti, G. (1983). Mechanisms of selective attention in mammals. In J.P. Ewert, R.R. Capranica, & D.J. Ingle (Eds), Advances in vertebrate neuroelhology. London: Plenum Press.
Rizzolatti, G. & Berti, A. (1990). Neglect as a neural representational deficit. Revue Neurologique, 146, 626–634.
Rizzolatti, G. & Camarda, R. (1987). Neural circuits for spatial attention and unilateral neglect. In M. Jeannerod (Ed.), Neurophysiological and neuropsychological aspects of neglect. Amsterdam: North-Holland.
Rizzolatti, G., Camarda, R., Fogassi, L. Gentilucci, M., Luppino. G., & Matelli. M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Experimental Brain Research, 71. 491 507.
Rizzolatti, G. & Gallese, V. (1988). Mechanisms and theories of spatial neglect. In F. Boiler & J. Grafman (Eds), Handbook of neuropsyehology. Vol. 1. Amsterdam: Elsevier.
Rizzolatti. G. & Gentilucci. M. (1988). Motor and visual-motor functions of the promotor cortex. In P. Rakic & W. Singer (Eds). Neurobiology of neocortex. Chichester: John Wiley.
Rizzolatti. G., Gentilucci. M., & Matelli. M. (1985). Selective spatial attention: One center, one circuit or many circuits? In M.I. Posner & O.M. Marin (Eds). Attention and performance, XI. Hillsdale, NJ: Lawrence Erlbaum Associates Inc.
Rizzolatti. G., Matelli, M. & Pavesi, G. (1983). Deficit in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in monkey. Brain, 106, 655 673.
Rizzolatti, G., Riggio, L., Dascola. I., & L’miltà, C. (1987). Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention. Neuropsychologia, 25, 31 - 40.
Robinson, D.L., McClurkin. J.W. & Kertzman. C. (1990). Orbital position and eye movement influences on visual responses in the pulvinar nuclei of the behaving macaque. Experimental Brain Research, 82, 235 -246.
Rubens, A.B. (1985). Caloric stimulation and unilateral visual neglect. Neurology, 35, 1019–1024.
Sakata, H., Shibutani, H., & Kawano, K. (1980). Spatial properties of visual fixation neurons in posterior parietal cortex of the monkey. Journal of Neurophysìology, 43, 1654–1672.
Shallice, T. (1988). From neuropsyehology to mental structure. Cambridge: Cambridge University Press.
Shelton, P.A., Bowers, D. & Heilman, K.M. (1990). Peripersonal and personal neglect. Brain, 113, 191–205.
Sherrington, C.S. (1906). The interactive action of the nervous system. London: Constable. (Second edition 1947, Cambridge, Cambridge University Press.)
Sprague. J.M. (1966). Interaction of cortex and superior colliculus in visually guided behavior in the cat. Science, 153. 1544–1547.
Stroop, J.R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643–662.
Taira, M., Mine, S., Georgopoulos, A.P., Murata, A., & Sakata, H. (1991). Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Experimental Brain Research, 83, 29–36.
Treisman, A.M. & Gelade, G. (1980). A feature-integration theory of attention. Cognitive Psychology. 12, 97–136.
Umiltá, C. (1988). Orienting of attention. In F. Boiler & J. Grafman (Eds), Handbook of neuropsyehology. Vol. I. Amsterdam: Elsevier.
Ungerleider, L.G. & Mishkin. M. (1982). Two cortical visual systems. In D.J. Ingle. M.A. Goodale. & R.J. Mansfield (Eds). The analysis of visual behavior. Cambridge, MA: MIT Press.
Volpe, B.T., Le Doux. J.E., & Gazzaniga. M.S. (1979). Information processing of visual stimuli in an extinguished field. Nature. 282, 722–724.
Young. A.W., de Haan, E.H.F., Newcombe, F., & Hay, DC (1990). Facial neglect. Neuropsychologia, 28. 391 415.
Zipser, D. & Andersen, A. (1988). A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature. 331. 679 684.