What kind of visual spatial attention is impaired in neglect?
Introduction
Unilateral spatial neglect is a widely known neuropsychological syndrome characterised by a severe impairment in detecting targets and initiating motor responses in contralesional space. The nature of this disorder is controversial (for recent reviews, see Heilman, Watson, & Valenstein, 2002; Kerkhoff, 2001, Vallar, 1998), but most researchers agree that it reflects deficits in spatial attention rather than in primary sensory or motor functions. One issue that is still at stake is whether such an impairment concerns mainly exogenous (stimulus driven, automatic) or endogenous (cognitively driven, controlled) attention. The balance of available evidence is in favour of an impairment of exogenous attention (e.g. Bartolomeo, Siérof, Decaix, & Chokron, 2001; Karnath, 1988; Ladavas, Carletti, & Gori, 1994; Losier & Klein, 2001; Luo, Anderson, & Caramazza, 1998; for a review, see Bartolomeo & Chokron, 2002), though there are data pointing to either a selective impairment of endogenous attention or of both forms of attention (see Corbetta, Kincade, & Shulman, 2002; Mesulam, 1999). In a previous study (Smania et al., 1998), we mapped the visual field distribution of spatial attention in neglect and extinction patients by using simple manual reaction time (RT) to a brief flash randomly presented to one location going from 40° contralesionally up to 40° ipsilesionally along the horizontal meridian. We found a dramatically asymmetric distribution of speed and accuracy of response around the vertical midline, with an increasingly slow RT in more peripheral parts of the contralesional hemifield and a paradoxical speeding in the ipsilesional side up to about 20° of stimulus eccentricity (see also Cavina-Pratesi et al., 2001). Since the sequence of stimulus presentation to the various field locations was unpredictable, attentional focusing was likely to be entirely stimulus driven. Therefore, we concluded that impairment in exogenous attention must have contributed to neglect patients’ abnormal field distribution of RTs. In a second experiment of the same study (Smania et al., 1998), we compared the performance of one neglect patient and one extinction patient under randomised versus blocked conditions. In the latter, stimuli were presented either to the same hemifield (for both patients) or to the same field point (for extinction patient only) throughout the whole experimental block and the patients could direct covert attention to the indicated side or location. The predictability of the hemifield of stimulus presentation yielded an overall decrease of RTs compared to randomised presentations in both patients; the patient with extinction also showed overall faster RTs in the blocked-point condition than in the blocked-hemifield and randomised conditions. However, the slopes of the eccentricity-RT curves of each patient were roughly similar across all conditions with a drastic increase in RT with eccentricity in the contralesional field and an essentially flat curve in the ipsilesional field. Those findings suggested that the two patients could benefit from prior knowledge of the side or location of the stimulus, even when it was presented in the contralesional hemifield, indicating a spared control of covert endogenous attention across the whole visual space which could not compensate for the dramatic inter-field asymmetry in the distribution of exogenous attention. In order to better substantiate such a preliminary evidence obtained from two patients only, in the present study, we decided to manipulate the expectancy of the spatial location of the impending stimulus in a similar manner as in the previous study and to directly examine the effects of exogenous and endogenous attention on a large sample of neglect patients as well as brain-damaged and elderly healthy controls (HC). This enabled us to verify whether the benefit from endogenous attention would be comparable in neglect patients and control subjects and to what extent it would modulate the abnormal visuo-motor performance of neglect patients typically observed with stimuli presented to unpredictable locations (e.g. De Renzi, Gentilini, Faglioni, & Barbieri, 1989; Ladavas, Petronio, & Umiltà, 1990; Smania et al., 1998). Furthermore, since most of neglect patients examined in our previous study (Smania et al., 1998) had an associated contralesional hemianopia, we wondered if this sensory impairment might have played a role in determining the abnormal distribution of attention in the intact ipsilesional hemifield. In order to verify that, in the present study, we separately analysed the performance of neglect patients with or without hemianopia as well as of a group of hemianopic patients (H) without neglect.
Disentangling the contribution of hemianopia to the neglect syndrome is a crucial issue and is still a matter of debate. Oculographic analyses have shown that during free viewing of simple visual patterns (Barton, Behrmann, & Black, 1998; Barton, Behrmann, Black, & Watt, 1997; Ishiai, Furukawa, & Tsukagoshi, 1989) or relatively complex visual displays (Behrmann, Watt, Black, & Barton, 1997), patients with hemianopia displayed more fixations toward the contralesional rather than the ipsilesional hemispace as was the case in patients with neglect. Moreover, it was observed in tasks of line bisection that, contrary to neglect patients whose subjective mid-point was deviated ipsilesionally, that of pure hemianopic patients was deviated contralesionally (Barton & Black, 1998; D’Erme, De Bonis, & Gainotti, 1987; Kerkhoff, 1993; see also the older German literature reviewed by Ferber & Karnath, 1999). These results suggest the presence of a directionally opposite deployment of spatial attention in hemianopics as compared to neglect patients with an attentional shift toward the contralesional rather than the ipsilesional hemispace in the former. This is likely to determine an opposite pattern of performance in the two groups even in simple perceptual-motor tasks. For example, an opposite performance in the judgement of the subjective straight ahead (SSA) in patients with hemianopia as compared to those with neglect has been found (Ferber and Karnath, 1999; Kerkhoff, Artinger, & Ziegler, 1999), with a contralesional or ipsilesional SSA displacement, respectively. Interestingly, Ferber and Karnath (1999) found no significant ipsilateral shift of SSA in a group of patients with neglect and additional hemianopia, their interpretation being that neglect and hemianopia interact so that their opposite biases neutralise each other. In contrast, the possibility that hemianopia might enhance rather than diminish neglect has been raised by Doricchi and colleagues (for a review, see Doricchi, 2002) on the basis of results indicating that the reversed form of misrepresentation of horizontal space typically observed in hemianopia without neglect in tasks of distance reproduction was frequently associated with neglect with hemianopia, rather than with neglect without hemianopia. These authors suggest that the apparent discrepancy of the results of Ferber and Karnath (1999) might simply depend on the specific methodology adopted to evaluate the straight-ahead position in their patients and that those findings could be reconciled with the hypothesis that hemianopia worsens rather than improve neglect (for details, see Doricchi, 2002).
Section snippets
Experiment 1
In Experiment 1, we aimed at ascertaining whether and to what extent in speeded light detection tasks neglect patients could benefit from eliminating the uncertainty of the location of the impending stimulus. We compared the performance of neglect patients with and without hemianopia with that of “pure” hemianopic patients, brain-damaged and elderly healthy controls in two conditions: in one, the blocked-point condition, the stimuli were presented within a given block of trials to one and the
Experiment 2
In Experiment 2, we aimed at investigating the possible influence of hemianopia on neglect by comparing the performance of N and NH patients in conditions where they could selectively attend to one hemifield only. This enabled us to study the differences in performance between the two groups in a given hemifield independently from the effect of presenting the stimuli to the other hemifield. Patients’ groups, stimuli and apparatus were the same as in Experiment 1, but we used a paradigm in which
Effects of endogenous focusing of attention on neglect patients’ performance
In Experiment 1, we found an overall effect of the predictability of the location of the impending stimulus on the performance of all groups, neglect patients included, with a speeding-up of RT in the blocked-point as compared to the randomised condition for both contralesional and ipsilesional presentations. This result, indicating a spared capability of selecting a location in the neglected contralesional hemifield and maintaining attention focused on it, confirms our preliminary observations
Acknowledgements
Part of this work was carried out in collaboration with Angelo Maravita, M.D. and Federica Romanelli, M.D. We are deeply indebted to Nicola Smania, M.D. and Silvia Berlucchi, M.D. for referring to us some of the patients tested in the present study. This work was funded by a COFIN grant from the Italian MURST and by a Marie Curie Fellowship of the European Community programme Quality of Life and Management of Living Resources under contract number QLG1-CT-2002-51552.
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