The Role of Spontaneous Eye Movements in Orienting Attention and in Unilateral Neglect
Institute of Neurology of the Catholic University of Rome, Rome, Italy
Introduction
Theories advanced to explain the unilateral neglect syndrome (see Bisiach & Vallar, 1988; De Renzi, 1982; Heilman, Valenstein, & Watson, 1985; Jeannerod, 1987; Weinstein & Friedland, 1977 and Gainotti, D’Erme, & De Bonis, 1989b for reviews) can be broadly classified into two major groups: (1) those that assume that neglect can be explained on the basis of peripheral input/output disturbances; (2) those that consider that disorders at a low level of integration cannot account for several aspects of this syndrome and propose that neglect must be traced back to a central (attentional or representational) disorder. In recent years, clinical and experimental data have convincingly shown, in agreement with the proponents of the second class of interpretations, that neglect phenomena cannot be reduced to disorders of gathering and processing sensory information. This suggests that peripheral factors only play a modulatory and not a causative role in unilateral neglect, and has oriented the interest of researchers almost entirely towards the central attentional and representational theories.
This attitude implies that peripheral and central factors are basically independent rather than strongly reciprocally interconnected. This view, however, is at variance with much data gathered both in normals and in brain-damaged patients, which seem to show that at least one of the peripheral factors (namely, the direction of spontaneous or automatic eye movements) exerts a strong influence upon the central attentional factors. The main scope of the present chapter will, therefore, consist in reviewing evidence supporting this line of thought. In particular, we will focus on a group of investigations prompted by the rather unexpected observation (Rubens, 1985) that severe manifestations of hemineglect can be dramatically improved (at least for short periods) by a caloric vestibular stimulation.
Our main thesis will be that the dramatic reduction of neglect observed after vestibular stimulation is the consequence of a peripheral reflex activity acting both with a direct and with an indirect mechanism. We assume that the facilitation of lateral gaze and head turning towards the neglected half-space (resulting from the elicitation of vestibulo-ocular and vestibulo-spinal reflex activities) can dramatically reduce unilateral neglect, not only because it allows a better visual exploration of the neglected half-space, but also (and perhaps even more) because it automatically orients attention in that direction.
The Sensorimotor Theories of Neglect
The most striking manifestations of neglect usually occur in right braindamaged patients showing a conjugate gaze deviation towards the right half-space, associated with left homonymous hemianopia and with left-sided somatosensory deficits. Some authors have assumed, therefore, that unilateral neglect may be but a consequence of these elementary sensori-motor disturbances, perhaps superimposed upon a background of widespread mental deterioration (Battersby, Bender, Pollack, & Kahn, 1956), which could prevent the patient from adopting adequate compensative strategies.
The best known instance of sensory defect hypothesis was presented by Denny-Brown, Meyer and Horenstein (1952), who proposed that the main function of the parietal lobes, usually severely damaged in neglect patients (Gainotti, 1968; Hecaen, 1962; Heilman, Valenstein, & Watson, 1983), may consist in synthesising the spatial aspects of the sensory stimuli. These authors, therefore, ascribed the neglect syndrome (which they called “amorphosynthesis”) to a defective spatial summation of multiple sensory data. Although usually considered as a theory viewing neglect as a consequence of a sensory defect, the high-level sensory integration taken into account here makes this hypothesis not too different from modern non-sensory theories. Another version of the sensory defect hypothesis has been proposed by Sprague, Chambers and Steller (1961) in an animal model of neglect provoked in the cat by interrupting the lateral portion of the mesencephalon. Since this part of the brain stem contains ascending sensory pathways, Sprague et al. (1961) concluded that unilateral neglect was due to a loss of patterned afferent input to the forebrain.
Several objections have been raised to these and to similar explanations of the neglect phenomena.
The defective exploration hypothesis stems from the observation that in the most severe forms of unilateral neglect, patients usually show a deviation of the head and eyes towards the lesion side and fail, for example, to orient towards a speaker addressing them from the contralateral half-space. Schott, Jeannerod and Zahin (1966), therefore, proposed that unilateral neglect might be the consequence of an oculomotor disorder, resulting from a disruption of automatic eye fixation mechanisms, preventing patients from fully exploring the contralateral half-space. More recently, De Renzi (1982) has also proposed that a limitation of eye movements towards the neglected half-space could partly explain unilateral neglect.
A more “central” and more sophisticated version of the defective exploration hypothesis has been proposed by Kinsbourne (1970; 1973; 1974; 1977), who has tried to explain neglect on the basis of an oculomotor imbalance mechanism. According to Kinsbourne, each hemisphere subserves orientation towards the contralateral half-space and tends, when activated, to direct the gaze towards the contralateral spatial field. In the intact brain, the balance between the two sides could be maintained through reciprocal trans-callosal inhibition, but two mechanisms could reduce the orientation tendencies towards the contralateral half-space in unilateral brain-damaged patients: (1) an increased level of trans-callosal inhibition exerted by the normal upon the damaged hemisphere; (2) a defective activation of the damaged hemisphere, diminishing the flow of excitation towards the corresponding orienting apparatus.
The net result of this inter-hemispheric imbalance would be a bias of head and gaze turning towards the half-space ipsilateral to the lesion side (see Chapter 3, this volume, for an overview of Kinsbourne’s conceptualisation of neglect and for a summary of the empirical data supporting his model). In more recent years, the hypothesis viewing unilateral neglect as a by-product of disrupted or imbalanced oculomotor mechanisms has been strengthened by the observation that conjugate eye defects, like unilateral spatial neglect, are more frequent and more lasting following right than left hemisphere stroke (De Renzi, Colombo, Faglioni, & Gibertoni, 1982; Mohr et al., 1984) and following right than left intracarotid sodium amytal injection (Meador et al., 1989). On the other hand, the hypothesis which views unilateral neglect as a consequence of a lost capacity to visually explore the contralateral half-space has also raised important objections:
Remission of Hemineglect During Vestibular Stimulation
As mentioned in the Introduction, great interest has been shown in recent years in Rubens’ (1985) observation that a caloric vestibular stimulation can provoke a transient but dramatic improvement of hemi-inattention in most neglect patients. Rubens, drawing on previous anecdotal observations by Silberpfennig (1941) and Marshall and Maynard (1983), studied the effects of caloric vestibular stimulation on gaze direction and on tests of visual neglect in a group of 18 right brain-damaged patients showing severe manifestations of hemineglect. He reasoned that, if visual neglect is partly due to a gaze and postural turning bias, then caloric vestibular stimulation, producing eye deviation and past-pointing in the direction opposite to this bias, should reduce signs of neglect. His results confirmed the hypothesis, since even in profound neglect patients the caloric-induced vestibular reflex significantly improved both the ability to gaze into the affected field and behaviour on tests of visual neglect.
These results have since been replicated and extended, using the same or similar methodologies, by other authors, who have shown that not only unilateral spatial neglect, but also other (possibly related) signs of right hemisphere damage, can be temporarily reduced by vestibular stimulation. Thus, Cappa, Sterzi, Vallar and Bisiach (1987) have shown that in addition to visual neglect, personal neglect and anosognosia can be temporarily alleviated by caloric vestibular stimulation and, even more recently, Vallar et al. (1990) have demonstrated that this improvement concerns both tasks performed under visual control and tasks performed without visual control. Furthermore, the same authors have shown that, at least in some patients, vestibular stimulation can temporarily reduce defects apparently due to “primary” sensory deficits, such as left hemianaesthesia.
On the other hand, Pizzamiglio et al. (1990) have demonstrated that a temporary reduction in hemineglect can also be obtained by using an optokinetic (instead of a caloric vestibular) stimulation, to provoke a nystagmus with a slow phase opposing the gaze bias shown by neglect patients.
It must be acknowledged, however, that if the remission of hemineglect during caloric vestibular stimulation and comparable manoeuvres is a well-established empirical fact, interpretations of this effect are still controversial. Neither Rubens (1985) nor the authors who have replicated and extended his findings, have entirely attributed the observed remission of hemineglect to an improved capacity to explore visually the half-space contralateral to the damaged hemisphere. Rubens, of course, explicitly assumed that this was the main mechanism, but (owing to the objections to the “defective exploration hypothesis” that we have just mentioned) also took into account the possible role of less elementary and more integrated mechanisms. One of these could be the influence that the vestibular input exerts upon the cortico-limbic-reticular system, implicated by Heilman and co-workers (e.g. Heilman & Valenstein, 1979; Heilman et al., 1985) in the maintenance of hemispheric arousal and readiness to respond to stimuli coming from the contralateral half-space. A second mechanism could consist in the modulation that the vestibular input exerts upon the visual cortical cells (Lahue, Reinis, Landolt, & Money, 1981) and upon the visual tracking neurons of the posterior parietal association cortex, since this modulation could facilitate the visual processing in the defective half-field.
Cappa et al. (1987), Pizzamiglio et al. (1990) and Vallar et al. (1990), on the other hand, were even more reluctant to admit that the effects of vestibular stimulation may be explained simply in terms of a facilitation of ocular movements towards the neglected side, since such a mechanism could not account for the improvement of personal neglect and the regression of anosognosia reported by Cappa et al. (1987), nor the temporary remission of hemianaesthesia and the improvement in extrapersonal neglect in the absence of visual control observed by Vallar et al. (1990). Pizzamiglio et al. (1990) gave a detailed description of the integrated neural mechanism fed by the vestibular system, drawing on a general theoretical model proposed by Jeannerod and Biguer (1987). These authors examined the process of building up the spatial map for directing movements towards the extrapersonal space, reviewing the contribution of eye position signals, head position signals and other signals in the construction of an egocentric body reference system.
They had considered unilateral neglect as an orienting bias produced by a lesion within this central representation of the body reference system, leading to an illusory rotation of the system of reference towards the lesion side. Pizzamiglio et al. (1990) assumed that the body-centred spatial map may be subserved and fed by redundant and independent proprioceptive, visual and vestibular subsystems, which do not need to be simultaneously activated. They proposed that a general imbalance of the spatial reference frame may be observed when a focal brain lesion disconnects this central integrative structure from one or more of the afferent subsystems. In this case, the activation of the remaining subsystems might be sufficient to reduce and partially compensate the spatial bias, which can be observed in a variety of tasks of space exploration.
We do not intend to enter here into a discussion of this explanation or of other similar interpretations. We will limit ourselves to the fact that if an improved visual exploration of the neglected half-space cannot explain phenomena such as the reduction of personal neglect, anosognosia. hemianaesthesia and so on. it is also unlikely that this set of phenomena may be explained by the improved functioning of a higher level integrative structure fed by the vestibular system. We therefore prefer to come back to the simpler and more parsimonious explanation, linking the reduction of hemineglect and of the associated signs of right hemisphere damage to the most obvious consequence of caloric vestibular stimulation, namely the facilitation of ocular movements towards the neglected side. We will propose that this very simple reflex mechanism can perhaps explain the whole set of phenomena observed by Rubens and by the authors who have replicated and extended his findings, provided the following additional assumptions are made:
The Influence of Attention Upon Signs of Right Hemisphere Damage Usually Associated with Neglect
The possibility that not only extrapersonal neglect, but also personal neglect (hemisomatoagnosia) and anosognosia, may be partly due to (or in any case influenced by) central attentional disorders has been repeatedly raised in the history of neuropsychology. Thus, Gentili (1965) maintained that right brain-damaged patients with anosognosia are unaware of their disability because they pay no attention to the left paralysed side of the body and a similar interpretation has been advanced by Critchley (1953) and Frederiks (1963) to explain personal neglect. Therefore, although it may be thought that a rather heterogeneous set of phenomena are described under the headings of anosognosia and of hemisomatoagnosia, it is likely that attentional factors usually interact with other somatosensory, representational and motivational factors in the production of these body-related behavioural disturbances. Even more likely is the link between left-sided anaesthesia and imbalanced distribution of attention, since increasing evidence in recent years has suggested that in right brain-damaged patients the processing of simple somatosensory stimuli may be influenced by high-level attentional factors. Thus, Weiskrantz and Zhang (1987) have shown that detection accuracy of stimuli applied to the left hand of a patient presenting a left-sided anaesthesia was modulated by the level of attention directed towards the stimulated hand. Stimuli were not detected when the patient was passively touched by the examiner on the left hand, but were much more frequently detected when she actively touched the left hand with her unaffected right hand or with a probe held by that hand. Tégner (1989) studied the response to tactile stimuli at the threshold range in two patients with chronic right parietal lesions. On the normal side, response thresholds were low and the number of correct responses increased steeply with increasing stimulus strength, whereas on the left side, the psychometric functions at the threshold range were much less steep and about 10% of the stimuli were not detected independent of the stimulus strength. Both these findings suggest that somatosensory deficits produced by right brain damage are modulated by central attentional factors.
Studies that have used double tactile simultaneous stimulation in various clinical and experimental situations give us further evidence in the same direction. These studies have shown that unilateral spatial neglect and tactile extinction on the body parts contralateral to the damaged hemisphere share important similarities with respect both to hemispheric asymmetries and to rehabilitation strategies. As for the first point, it has been shown that contralateral tactile extinction is more frequent and severe following right than left brain damage both in conditions of spontaneous brain pathology (Gainotti, De Bonis, Daniele, & Caltagirone, 1989a) and after intracarotid amytal injection (Meador & Heilman, 1988). As for the second point, Nocentini, Troisi, Carlesimo and Caltagirone (1990) have recently shown that rehabilitation techniques aiming at ameliorating unilateral spatial neglect by intensively training patients to orient attention towards left half-space also significantly reduce the incidence of contralateral tactile extinctions.
Now, if we accept that anosognosia, personal neglect and somatosensory defects may be due in part to the defective attention paid to the left side of the body, it becomes possible to assume that vestibular stimulation may temporarily ameliorate these symptoms by directing attention towards the left side of personal and extrapersonal space.
Direction of Spontaneous or Automatic Eye Movements and Spatial Orienting of Attention
Although several experiments have shown that attention can be allocated to different parts of the spatial field without making overt eye movements (for reviews, see Posner, 1980; Umiltà, 1988), this does not mean that independent processes are involved in the generation of eye movements and in the spatial allocation of attention. Experiments performed in normals by Crovitz and Daves (1962), Remington (1980) and Shepherd, Findlay and Hockey (1986) suggest, for example, a close relationship between eye movements and displacements of attention. In particular, the results obtained by Sheperd et al. (1986) suggest an asymmetric relationship between the two phenomena, since they indicate that it is possible to move attention without making eye movements, but it is not possible to make an eye movement without shifting in the same direction the focus of attention.
It must also be considered that both in experimental and in more ecological situations, effortful and highly controlled operations are necessary to obtain a dissociation between eye movements and spatial allocation of attention, whereas in more spontaneous or automatic conditions, close co-ordination between eye movements and displacements of attention seems essential for a smooth performance. Thus, both experimental data and commonsense considerations suggest that the direction of eye movements usually prompts a corresponding spatial orientation of attention. This suggestion is supported by a consistent body of data obtained in normals and in brain-damaged patients.
Data Gathered in Normals
Gopher (1973) was the first to observe that during dichotic listening tasks, the eyes of subjects tended to orient to and to remain fixated in the direction of the relevant ear and suggested that these eye movements oriented the subjects’ attention towards the appropriate part of space. Gopher also noted that the right ear advantage usually observed in verbal dichotic listening tasks increased by directing the gaze towards the right half-space, but disappeared by inverting the direction of gaze (Gopher, 1971, cited in Honoré, Bourdeaud’hui, & Sparrow, 1989). Similar results were obtained by Larmande et al. (1983; 1984) using non-verbal sounds as stimuli, which in a dichotic listening paradigm usually give a left ear advantage. In this case, too, the direction of gaze influenced the spatial allocation of attention, as the left ear advantage was increased by directing the gaze towards the left and reversed by orienting the gaze towards the right. Results obtained by Honoré (1982) when studying the detection of tactile stimuli, are also consistent with the hypothesis of a link between direction of eye movements and spatial allocation of attention. Honoré noted that the detection rate of cutaneous stimuli was higher and the reaction times were shorter when the eyes were turned towards the side stimulated by the examiner.
It must be noted, however, that not all the authors who have performed the above-mentioned experiments have interpreted their data as indicative of a link between direction of gaze and spatial allocation of attention. Larmande et al. (1983; 1984), in particular, have interpreted their data within the theoretical framework proposed by Kinsbourne (1970; 1974; 1977). They assumed that the act of turning the eyes towards one half of space (e.g. the left side) increases the level of activation of the corresponding hemisphere (in this case the right one), thus improving the processing of information coming from the contralateral space (and hence from the left ear) at the expense of stimuli presented at the right ear. This interpretation, which assumes an indirect link (via activation of the contralateral hemisphere) between direction of eye movements and efficiency of performance accomplished in the corresponding spatial field, has recently been tested by Honoré et al. (1989). Among normal subjects examined in a darkened room, Honoré et al. measured reaction times to lateral cutaneous stimulations, when the eyes were directed (a) towards the stimulated area, (b) towards another point within the same hemispace and (c) towards the opposite hemispace. Cutaneous reaction times were shortened only when the stimulation occurred at the centre of the area where the gaze was directed, but not when it occurred at any other point in the same hemispace. These data clearly suggest that eye movements facilitate the processing of stimuli occurring at the centre of the virtual visual field because of a correlative displacement of attention and not because of a resulting activation of the corresponding hemisphere.
Data Gathered in Brain-Damaged Patients
Three sets of data obtained in brain-damaged patients are consistent with the hypothesis that the direction of gaze automatically prompts a corresponding displacement of attention.
Among 10 right brain-damaged patients, Larmande and Cambier (1981) studied the incidence of tactile extinction on the left side of the body under various experimental conditions. The lateral orientation of gaze proved to be the most effective variable, as the incidence of extinction decreased when the gaze was oriented towards the left half-space and increased when it was directed to the right. The authors attributed these findings to the hemispheric activation provoked by the act of turning the eyes towards the contralateral half-space; however, the fact that language activities, which certainly induce a left hemisphere activation, were much less effective in increasing the incidence of tactile extinction, weakens this interpretation.
Benin. Perrier, Cambier and Larmande (1988) submitted two patients presenting a pathological gaze deviation towards the right side as a consequence of a brain stem lesion to a non-verbal dichotic listening task. Contrary to what is usually observed in normal conditions, but in agreement with the direction of the pathological gaze deviation, the number of first answers and the overall number of correct responses were greater for the right than for the left ear.
Meador et al. (1987) studied what influence turning the head and eyes of the patient to the right or left side can have upon the severity of neglect observed in a representative task. Their patient, who had lived in the same neighbourhood for over 20 years and who had a thorough knowledge of the families and houses near his home, was asked to imagine (while he was looking straight ahead at the examiner) that he was standing at the end of the street leading to his house.
With this mental set established, he was requested to name the houses on the street. Almost all the houses recalled were in the imagined right half-space, whereas very few were in the left half-space. When, however, he was re-tested with his eyes/head rotated to the left, recall of items lying in the left hemispace improved significantly. Thus, clinical observations and experiments accomplished in normal subjects and in brain-damaged patients consistently show that the direction of eye movements leads to a corresponding spatial orienting of attention. This effect is observed in different types of lateral eye deviation: when this posture is actively assumed by the subject (as in Larmande and co-workers’ studies); when it is a consequence of a brainstem lesion producing a pathological gaze deviation (as in Benin and co-workers’ study); and when the examiner physically turns the eyes/head of the patient (as in Meador and co-workers’ study).
The results of this last investigation are also interesting because they suggest that the direction of gaze is not the only factor which prompts a consensual automatic displacement of attention. Other components of the orienting reaction, such as head turning and trunk turning, are probably part of the same phenomenon, namely an automatic movement of attention towards the part of space pointed at by the body-orienting apparatus. This position, which is in agreement with the recent results of Karnath, Schenkel, and Fischer (1990) that the spatial trunk orientation is an important determining factor of contralateral neglect, is not inconsistent with the results of the caloric vestibular stimulation. The latter, in fact, produces an integrated pattern of reflex activities (comprising the vestibulo-ocular and the vestibulo-spinal reflexes), which synergically orient in the same direction the gaze, head and trunk of the subject.
Implications for Theories of Unilateral Neglect
In previous sections of this chapter, we have tried to demonstrate that lateral eye movements (and the turning movements of the body-orienting apparatus in general) lead to an automatic dislocation of attention towards the corresponding parts of personal and extrapersonal space. We have also suggested that a facilitation of ocular movements and of head turning towards the neglected half-space can explain the transient but dramatic improvement of neglect and of related phenomena observed after vestibular caloric stimulation. These findings, which cannot be simply attributed to an improved visual exploration of the neglected half-space, have been interpreted as the consequence of a less imbalanced distribution of attention, allowing the patient to allocate attention automatically not only to the right, but also to the left half of personal and extrapersonal space.
Our interpretation of the above-mentioned data suggests that the mechanisms disrupted in unilateral neglect are seemingly located within a circuit connecting the central and the peripheral components of a structure subserving the spatial automatic displacements of attention, but does not necessarily point to the more central or to the more peripheral components of this circuit. Various general theories of neglect are, therefore, compatible with our interpretation. Thus, the stress put on the reciprocal interconnections between eye movements and movements of attention could increase the explanatory power of theories suggesting that an elementary oculomotor disorder might play a critical role in unilateral spatial neglect. On the other hand, the automatic nature of the attentional displacements prompted by lateral eye movements could suggest that the attentional bias in unilateral neglect mainly concerns the automatic, rather than the intentional, allocations of attention. This is in line with the view, advanced in previous papers (Gainotti et al., 1989b; Gainotti, D’Erme, & Bartolomeo, 1991), that unilateral neglect may be due to a selective disruption of mechanisms provoking an automatic orienting of attention towards the contralateral half-space, with relative sparing of mechanisms subserving volitional orienting of attention. Similar viewpoints are put forward in this book by Humphreys and Riddoch (Chapter 7) and by Làdavas (Chapter 9).
Finally, our interpretation of the vestibular stimulation experiments is compatible with those theories that assume that more “central” mechanisms of attention are disrupted in unilateral neglect. It is. for example, certainly consistent with Kinsbourne’s theory, which views neglect as the consequence of a gaze and postural bias towards the half-space ipsilateral to the lesion side (Kinsbourne, 1977; 1989). It must be added, however, that although it is compatible with all these theories, our interpretation remains neutral as regards the mechanisms proposed to account for one of the most striking aspects of unilateral spatial neglect, namely its prevalence in patients with right hemisphere damage (for reviews, see Bisiach & Vallar, 1988; De Renzi, 1982; Gainotti et al., 1989b; Heilman et al., 1985). Our interpretation of the results obtained with caloric vestibular stimulation can, indeed, be equally well accommodated by: (a) the hypothesis advanced by De Renzi et al. (1982) that the prevalence of neglect in right brain-damaged patients may be due to a right hemisphere superiority for oculomotor functions; (b) our hypothesis which assumes that right hemisphere organisation may be more strongly dependent upon automatic forms of orienting reactions and that therefore a right brain lesion may more easily produce a strongly ipsilaterally imbalanced orienting bias (Gainotti et al., 1991); (c) Kinsbourne’s hypothesis, viewing the prevalence of neglect for the left half-space as the exaggeration of a physiological asymmetry, leading normal subjects to orient preferentially towards the right half-space (Kinsbourne, 1987); and (d) Heilman’s theory, which considers the prevalence of unilateral neglect in right brain-damaged patients to be due to the different organisation of the receptive fields of right and left parietal attentional neurons (Heilman & Valenstein, 1979; Heilman & Van Den Abell, 1980; Heilman et al., 1985).
The importance of vestibular stimulation experiments for theories of hemineglect must, therefore, be neither underestimated nor overestimated. Although they restrict the strongest candidates to theories which stress central or peripheral aspects of the lateral orienting of attention, they must also be integrated with other data to check for more specific aspects of these different theories, so as to allow for a more precise understanding of the nature of unilateral neglect.
References
Albert, M.L. (1973). A simple test of visual neglect. Neurology, 23. 658–664.
Battersby. W.S., Bender, M.B., Pollack, M., & Kahn, R.L. (1956). Unilateral spatial agnosia (inattention) in patients with cerebral lesions. Bruin, 79, 68–93.
Benin, C., Perrier, D., Cambier, J., & Larmande, P. (1988). Influence de la déviation pathologique du regard par lésion du tronc cérébral sur Iéquilibre inter hémispherique. étudié par le test d’écoute dichotique non verbal. Neuropsychologia, 26. 753–758.
Bisiach, E., Capitani, E., Luzzatti, C, & Perani, D. (1981). Brain and conscious representation of outside reality. Neuropsychologia. 19. 543–551.
Bisiach, E. & Luzzatti, C. (1978). Unilateral neglect of respresentational space. Cortex. 14. 129–133.
Bisiach, E. & Vallar, G., (1988). Hemineglect in humans. In F. Boiler & J. Grafman (Eds). Handbook of neuropsychology. Vol. 1. Amsterdam: North-Holland.
Bisiach, E., Vallar, G., Perani, D., Papagno, C, & Berti. A. (1986). Unawareness of disease following lesions of the right hemisphere: Anosognosia for hemiplegia and anosognosia for hemianopia. Neuropsychologia. 24, 471 -82.
Cappa. S., Sterzi, R., Vallar. G., & Bisiach. E. (1987). Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia. 25. 775–782.
Chedru, F. (1976). Space representation in unilateral spatial neglect. Journal of Neurology, Neurosurgery ami Psychiatry, 39. 1057–1061.
Critchley, M. (1953). The parietal lobes. New York: Hafner.
Crovitz. H.F. & Daves, W. (1962). Tendencies to eye movements and perceptual accuracy. Journal of Experimental Psychology, 63. 495–498.
Denny-Brown, D., Meyer. J.S., & Horenstein. S. (1952). The significance of perceptual rivalry resulting from parietal lesions. Brain. 75, 433 471.
De Renzi, E. (1982). Disorder of space perception and cognition. New York: John Wiley.
De Renzi, E., Colombo. A., Faglioni. P., & Gibertoni, M. (1982). Conjugate gaze paralysis in stroke patients with unilateral damage. Archives of Neurology, 39, 482–486.
De Renzi. E., Faglioni. P., & Scotti. G. (1970). Hemispheric contribution to the exploration of space through the visual and tactile modalilty. Cortex, 6, 191–203.
D’Erme, P., De Bonis. C., & Gainotti. G. (1987). Influenza dell’emi-inattenzione e deH’emianopsia sui compiti di bisezione di linee nei pazienti cerebrolesi. Archivio Ji Psicologia. Neurologia e Psichialria. 3H, 193–207.
Frederiks, J.A.M. (1963). Anosognosie et hémiasomatognosie Revue Neurologic/iie, 109, 585–597.
Gainotti, G. (1968). Les manifestations de negligence et d’inattention pour 1’hémispace. Cortex. 4, 64–91.
Gainotti, G., De Bonis. C., Daniele. A., & Caltagirone, C. (1989a). Controlateral and ipsilateral tactile exinction in patients with right and left focal brain damage. International Journal of Neuroscience, 45. 81–89.
Gainotti, G., D’Erme, P., & Bartolomeo. P. (1991). Early orientation of attention toward the half space ipsilateral to the lesion in patients with unilateral brain damage. Journal of Neurology, Neurosurgery and Psychiatry, 54, 1082–1089.
Gainotti, G., D’Erme, P., & De Bonis, C. (1989b). Components of visual attention disrupted in unilateral neglect. In J.W. Brown (Ed.), Neuropsvchology of visual perception, pp. 123–144. Hillsdale, NJ: Lawrence Erlbaum Associates Inc.
Gentili, C. (1965). Corpo come relazione. Sistema Nervoso, 17, 174–187.
Gentilini, M., Barbieri, C., De Renzi. E., & Faglioni, P. (1989). Space exploration with and without the aid of vision in hemisphere-damaged patients. Cortex, 25, 643–651.
Gopher, D. (1973). Eye-movement patterns in selective listening tasks of focused attention. Perceptual Psychophysics, 14, 259–264.
Haliigan. P.W., Marshall, JC & Wade, D.T. (1990). Do visual field deficits exacerbate visuo-spatial neglect? Journal of Neurology, Neurosurgery and Psychiatry, 53, 487–491.
Halsband, U., Gruhn, S., & Ettlinger, G. (1985). Unilateral spatial neglect and defective performance in one half of space. International Journal of Neuroscience, 28. 173–195.
Hécaen, H. (1962). Clinical symptomatology in right and left hemisphere lesions. In V.B. Mountcastle (Ed.). Interhemispheric relation ami cerebral dominance. Baltimore, MD: Johns Hopkins University Press.
Heilman, K.M. & Valenstein, E. (1979). Mechanisms underlying hemi-spatial neglect. Annals of Neurology. 5, 166–170.
Heilman, K.M., Valenstein, E., & Watson, R.T. (1983). Localization of neglect. In A. Kertesz (Ed.). Localization in neuropsvchology (pp. 371–392). New York. NY: Academic Press.
Heilman, K.M., Valenstein. E., & Watson. R.T. (1985). The neglect syndrome. In P.J. Vinken. G.J. Bruyn & H.L. Klawans (Eds), Handbook of clinical neurology: Vol. 45 (pp. 152–183). Amsterdam: Elsevier Science Publishers.
Heilman, K.M. & Van den Abell, T. (1980). Right hemispheric dominance for attention: The mechanism underlying hemispheric asymmetries of inattention (neglect). Neurology, 30, 327–330.
Honoré. J. (1982). Posture oculaire et attention sélective a des stimuli cutanes. Neuropsychologia, 20. 727–730.
Honoré, J., Bourdeaud’hui, M., & Sparrow, L. (1989). Reduction of cutaneous reaction time by directing eyes towards the source of stimulation. Neuropxycltologia, 27, 3. 367–371.
Ishiai, S., Furukawa, T., & Tsukagashi, H. (1987). Eye-fixation patterns in homonymous hemianopia and unilateral spatial neglect. Neuropsychologia, 25, 675–679.
Jeannerod. M. (Ed.) (1987). Neurophysiologkal and neurapsycholagtcal aspens of spatial neglect. Amsterdam: North-Holland.
Jeannerod. M. & Biguer, B. (1987). The directional coding of reaching movements. In M. Jeannerod (Ed.), Neurophysiologkal and neuropsychologhal aspects of spatial neglect, pp. 87–113. Amsterdam: North-Holland.
Karnath. H.O., Schenkel, P., & Fischer. B. (1990). Trunk orientation as a determining jailor of “contra/ateral” deficit in neglect. Paper presented at the 8th European Workshop on Cognitive Neuropsychology, Bressanone. January.
Kinsbourne. M. (1970). A model for the mechanism of unilateral neglect of space. Transactions of the American Neurological Association. 95, 143.
Kinsbourne. M. (1973). The control of attention by interaction between the cerebral hemispheres. In S. Kornblum (Ed.). Attention and performance IV. New York: Academic Press.
Kinsbourne, M. (1974). Direction of gaze and distribution of cerebral thought processes. Neuropsychologia. 12. 270–281.
Kinsbourne, M. (1977). Hemineglect and hemispheric rivalry. In E.A. Weinstein & R.P. Friedland (Eds). Advances in neurology. Vol. 18. New York: Raven Press.
Kinsbourne, M. (1987). Mechanisms of unilateral neglect. In M. Jeannerod (Ed). Ncurophy-siological and neuropsychologieal aspects of spatial neglect, pp. 69 86. Amsterdam: North-Holland.
Lahue, B.H., Reinis. S., Landolt. J.F., & Money. K.E. (1981). Visual vestibular interactions in visual cortical cells in the cat. Annals of the New York Academy of Sciences. 374. 262–273.
Larmande, F., Elghori. D., Sintes. J., Bigot. Th., & Autret. A. (1983). Test d’écoute dichotique verbal et non verbal chez le sujet normal: influence de létat d’activation hémisphérique. Rente Neurologique, 139. 65–69.
Larmande, P., Blanchard. F., Sintes, J., Belin. C. & Autret. A. (1984). Test d’ecoute dichotique melodique. Influence de 1’etat d’activation hemispherique chez les sujets normaux, musiciens et non musiciens. Revue Nvwologique. 140. 49 54.
Larmande. P. & Cambier, J. (1981). Influence de létat d’activation hémisphérique sur le phénoméne d’extinction sensitive chez 10 patients atteints de lésions hemispheriques droites. Revue Newologique, 137, 285- 290.
Marshall, C.R. & Maynard. R.M. (1983). Vestibular stimulation for supranuclear gaze palzy: Case Report. Archives of Physical Medicine and Rehabilitation. 64. 134–146.
Meador. K.J. & Heilman, K.M. (1988). Right cerebral specialization for tactile attention as evidenced by intracarotid sodium amytal. Neurology. 38. 1763–1766.
Meador, K.J., Loring, D.W., Bovvers. D., & Heilman. K.M. (1987) Remote memory and neglect syndrome. Neurology. 37, 522 536.
Meador, K.J., Loring, D.W., Lee. G.P., Brooks. B.S., Nichols. F.T., Thompson. E.E., Thompson. W.O., & Heilman, K.M. (1989). Hemisphere asymmetry for eye gaze mechanisms. Brain. 112, 103–111.
Meienberg, O., Harrer, M., & Wehren. C. (1986) Oculographic diagnosis of hemineglect in patients with homonymous hemianopia. Journal of Neurology. 233. 97–101.
Meienberg, O., Zangemeister. W.H., Rosenberg. M., Hoyt. W.F., & Stark, L. (1981). Saccadic eye movement strategies in patients with homonymous hemianopia. Annals of Neurology. 9. 537–544.
Mohr, J.P., Rubinstein, L.V., Kase, C.S., Price, T.R., Wolf, P.A., Nichols, F.T., & Tatemichi, T.K. (1984). Gaze palsy in hemispheral stroke: The NINCDS Stroke Data Bank, Neurology, 34, 199 (suppl. 1).
Nocentini, U., Troisi, E., Carlesimo, G.A., & Caltagirone, C. (1990). Cognitive rehabilitation of hemi-inallentive disorders. Communication to the 3rd International S1STED Conference, Bologna, April.
Pizzamiglio, L., Frasca, R., Guariglia, C., Incaccia, R., & Antonucci, G. (1990). Effect of optokinetic stimulation in patients with visual neglect. Cortex, 26, 534–540.
Posner, M.I. (1980). Orienting of attention: The Vllth Sir Frederic Bartlett Lecture. Quarterly Journal of Experimental Psychology, 32, 3–25.
Remington, R.W. (1980). Attention and saccadic eye movements. Journal of Experimental Psychology, 6, 726–744.
Rubens, A.B. (1985). Caloric stimulation and unilateral visual neglect. Neurology, 35, 1019–1024.
Schott, B., Jeannerod, M., & Zahin, M.A. (1966). L’agnosie spatiale unilatéral: perturbation en secteur des méchanismes d’exploration et de fixation du regard. Journal de Medicine de Lyon, 47, 169–195.
Shepherd, M., Findlay, J.M., & Hockey, R.J. (1986). The relationship between eye movements and spatial attention. Quarterly Journal of Experimental Psychology, 38A, 475—491.
Silberpfennig, J. (1941). Contributions to the problem of eye movements. III. Disturbances of ocular movements with pseudohemianopia in frontal tumors. Confinia Neurologica, 4, 1–13.
Sprague, J.M., Chambers, W.W., & Steller, E. (1961). Attentive, affective and adaptive behavior in the cat. Science, 133, 165–173.
Tegner, R. (1989. Tactile sensibility in parietal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 52, 669–670.
Umilta, C. (1988). Orienting of attention. In F. Boiler & J. Grafman (Eds), Handbook of neuropsychology. Vol. 1. Amsterdam: North-Holland.
Vallar, G., Sterzi, R., Bottini, G., Cappa, S., & Rusconi, L. (1990). Temporary remission of left hemianaesthesia after vestibular stimulation. A sensory neglect phenomenon. Cortex, 26, 123–131.
Weinstein, E.A., & Friedland, R.P. (1977). Hemi-inattention and hemisphere specialization. New York: Raven Press.
Weintraub, S. & Mesulam, M.M. (1987). Right cerebral dominance for spatial attention: Further evidence based on ipsilateral neglect. Archives of Neurology, 44, 621–625.
Weiskrantz, L. & Zhang, D. (1987). Residual tectile sensitivity with self-directed stimulation in hemianaesthesia. Journal of Neurology, Neurosurgery and Psychiatry, 50, 632–64.