Brain Advance Access originally published online on December 14, 2007
Brain 2008 131(5):e95; doi:10.1093/brain/awm274
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Reply: no reversal of the Oppel–Kundt illusion with short stimuli: confutation of the space anisometry interpretation of neglect and ‘crossover’ in line bisection
Department of Neurological and Vision Sciences, University of Verona, Italy
Correspondence to: Silvia Savazzi, Dept. of Neurological and Vision Sciences – Sect. of Physiology, University of Verona, Strada le Grazie, 8 37134 Verona, Italy E-mail: silvia.savazzi{at}univr.it
Sir, neglect is a phenomenon that is both equally fascinating and equally controversial, as evidenced by the response of Doricchi et al. to our recently published paper in ‘Brain’ that detailed a series of five studies testing the space anisometry hypothesis of neglect. Doricchi and colleagues argue that our conclusions are incorrect for two main reasons. First, they follow up on our Experiment 1 with neurologically intact individuals and claim to demonstrate that the crossover effect that we found in our controls (age-matched to our patient population) is not observed with a larger sample of control participants. Second, they argue that the crossover effect we observed is likely to result from compensatory fixations to the contralateral hemi-field that is induced by hemianopia. I address each of these criticisms in turn.
As consistently pointed out by Doricchi et al., patients with neglect and concomitant hemianopia typically display a stronger crossover effect compared with the performance of neglect patients without hemianopia (Doricchi et al., 2005
). Hence, this effect and the extensive evidence that the presence of a visual field defect has a strong impact in worsening the rightward shift of line bisection errors in neglect with long lines (e.g. Harvey et al., 1995; Doricchi and Angelelli, 1999; Harvey and Milner, 1999; Doricchi et al., 2002a, b, 2003; Savazzi et al., 2004), suggest a strict and predictable relationship between the rightward bias in bisecting long lines and the crossover effect in bisecting very short lines: the stronger the ipsilesional bisection error with long lines, the stronger the contralesional bisection error with short lines. I suggest that Doricchi et al. did not replicate our results with neurologically intact individuals because they exhibited a weaker rightward bias in bisecting long lines than did our sample, which precluded them from observing the crossover effect. Comparing the results reported by Doricchi et al. in their correspondence and the ones of the first experiment in our study, a difference in the strength of the illusory effects emerges (Table 1).
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With lines 160 mm long, the strength of the Oppel–Kundt illusion is weaker in the sample data by Doricchi et al., both for the Left-Longer and the Right-Longer conditions. This holds true, not only with regard to the actual bisection performance (first column), but also if the illusion is calculated as deviation in bisection performance for both the Empty and the Filled conditions. Remarkably, with regards to the Right-Longer conditions (that is, the condition thought to resemble the horizontal space distortion in neglect) calculated as deviations to the Filled stimuli (rightmost column; ‘which represents the most appropriate comparative baseline for stimuli with anisometrically spaced inducers,’ as correctly suggested by Doricchi et al.), one can see that the difference in the strength of the illusion in the two studies is the greatest (3.48 mm). Hence, this comparative analysis provides a plausible reason for the differences obtained in their study with healthy subjects and ours. The strict and direct relationship between the ipsilesional bisection error with long lines and the crossover effect with short lines, could, thus, explain the lack of illusory inversion found by Doricchi and colleagues: a weaker rightward deviation of the bisection mark with long lines could have had the effect of reducing the probability to find an inversion of the deviation with short lines. Thus, the null results of Doricchi and colleagues may have resulted from characteristics of their particular sample as compared to ours—that is a group of individuals weakly prone to the illusion.
Regardless of the nature of the differences between the two studies, the results of the other experiments in our paper do not hinge on the results of our first experiment as claimed by Doricchi et al. They describe the results of our Experiment 1 and state that they ‘represent the founding empirical premise on which the rationale and conclusions of [our] study is entirely based.’ This is not the case. Our rationale is based on a long series of studies performed by Bisiach and colleagues (1994, 1996, 1997, 1998, 1999, 2002; Ricci et al., 2004; Savazzi et al., 2004), which have clearly articulated the space anisometry hypothesis and provided empirical validation, raising it much above the level of a ‘the purely metaphorical interpretation of clinical evidence offered by the space anisometry hypothesis’ as argued by Doricchi and colleagues. In fact, the hypothesis is quite computationally specific providing a quasi-mathematical description of how the representation of space is distorted in these patients, accounting also for the findings of other authors in different tasks and sensory modalities (e.g. Milner et al., 1993; Milner and Harvey 1995; Chokron et al., 1997; Milner et al., 1998; Irving-Bell et al., 1999; Ricci et al., 2000; Harvey et al., 2001, 2007).
Furthermore, we do not believe that the results of studies with neurologically intact individuals can refute theories of neglect; rather they can only help to corroborate them as a plausible explanation. We provide the data of Experiment 1 as converging evidence for our studies of patients with neglect. Doricchi et al. argue, however, that their null findings of an inversion of the effect of the Oppel–Kundt illusion with very short lines and ‘all of the findings reported in literature (Long and Murthagh, 1984; Bulatov and Bertulis 1997; Bulatov et al., 1999; Bertulis and Bulatov, 2005) ... unequivocally confute the space anisometry interpretation of spatial neglect behavior and cross-over effect in line bisection.’ However, we do not believe that results from intact individuals can refute explanations of a clinical syndrome. For example, consider a well-regarded hypothesis regarding neglect that of the attentional gradient put forth by Kinsbourne (1970). He has postulated that there are two competing attentional biases, each one separately controlled by the contralateral hemisphere and they differ in strength (i.e. stronger towards the right side of space). Such a theory predicts that healthy subjects should display a slight but rightward error in bisecting a line. But in actuality, one typically observes a slight but significant leftward error (the so-called pseudo-neglect phenomenon, e.g. Bowers and Heilman, 1980; Jewell and McCourt, 2000). It would seem a bit far-fetched to refute this theory only on the basis of results with neurologically intact individuals.
With regards to the second point, I agree with Doricchi et al. claiming that, as a consequence of hemianopia, ‘compensatory fixations toward the blind contralesional hemifield’ can explain ‘the strong cross-over effect found in N+H+ patients.’ However, although such compensatory contralesional fixations can explain the ‘worsening’ of the contralesional errors, they cannot explain the crossover per se. Most importantly, we even observed the crossover effect in patients without hemianopia in our study (Savazzi et al., 2007). Thus although hemianopia may increase the crossover effect, it cannot explain it: the presence of crossover in neglect patients without hemianopia disproves the compensatory contralesional fixations as having a causal role in the genesis of such an effect. Rather, I argue that the space anisometry hypothesis provides an adequate and comprehensive explanation for the crossover effect in neglect patients with and without hemianopia.
In this respect, it is important to note that the predictions of the space anisometry hypothesis are not as strict as stated by Doricchi and colleagues (‘It is clear that this hypothesis predicts that at any point in the gradient and for any length of a line set within this gradient, the line's left side will always be perceived as being shorter than its identical right counterpart and the subjective line midpoint will always be shifted rightward’). In fact, (as my ‘mentor’ Edoardo Bisiach always reminded me) this hypothesis postulates that (i) the within- and between-object relationships are transiently represented, thus changing over time and, more importantly; (ii) the strength of the spatial distortion, and thus its impact on the patients’ behaviour, can be different depending on the severity of neglect and the requirements of the task. With regard to the crossover effect, if space in neglect is represented consistently with the effect of the Oppel–Kundt illusion, the predictions of the space anisometry hypothesis depend on the strength of such an illusion with lines of different length. To explain crossover, then, neglect patients are expected to have a reduction of the illusory effect with a reduction in line length so that with very short lines, the effect is reversed (which is exactly what we have observed in Experiments 2, 3 and 5 of our study).
Two further issues raised by Doricchi and colleagues merit some consideration: the formula used in our study to draw the stimuli and our reference to the work by Bulatov and colleagues. As for the formula used in our paper and in the present correspondence, Doricchi and colleagues have correctly and carefully used our procedure to prepare the stimuli. Doricchi and colleagues have also interestingly added a new type of stimuli, that is, a version of the Oppel–Kundt illusion not enclosed in rectangles. Unfortunately, having not reported the results separately for the two conditions, I have to infer that the authors did not find any difference in the effect of the Oppel–Kundt illusion on line bisection errors (the same seems to be true for the two groups of subjects of different age). Importantly, however, it should be noted that the exact formula used is not crucial to obtaining the results we report. The results reported in our recent paper on 21 neglect patients (presented as a group average, Savazzi et al. 2007) and two previous experiments (Ricci et al., 2004; Savazzi et al., 2004) using different formulas, have found a reliable and consistent effect on the patients’ behaviour that is in accord with the predictions of the space anisometry hypothesis. It should be noted that there can be individual variations in the strength of that illusion, depending on the strength of the distortion of the spatial representation caused by the brain damage, which is clearly demonstrated in the paper by Ricci et al. (2004) in which such illusory effects are reported separately for each patient (Table 2, p. 230).
As for the studies by Bulatov and colleagues, we agree with Doricchi and colleagues that in these papers the authors did not find an inversion of the illusion for very short lines. This is exactly what it is reported in our paper ‘The authors (Bulatov et al. 1997; Bulatov and Bertulis, 1999) ... found that size of comparison errors (that is the measure of the distortion of length perception induced by the illusion) decreased with decreasing length of reference stimulus’; and also that the data ‘found in the present experiment (Savazzi et al., 2007) ... provide the additional information that this distortion of space affects where the midline is perceived to be.’ In this respect, we did not stress our conclusions on healthy subjects with reference to these studies for the following important reasons that made these studies not correctly comparable. Firstly, as suggested by Doricchi et al., two very different tasks were used: a visuo-motor task in our paper and a purely psychophysical task in the papers by Bulatov and colleagues. Secondly, only in the studies by Bulatov and colleagues was the actual size of the stimuli experimentally controlled by means of the use of a monitor and a chin-rest to have the same distance between the neurologically intact subjects and the stimulus. Instead, our study and in the one by Doricchi et al. the experiments were carried out with an undefined ‘reading distance’, because of which the actual size of the stimuli might change trial by trial simply because of changes in the distance of the patient from the paper. These two procedural differences may possibly explain the difference in their results and ours. Importantly, however, we used the same procedures in our healthy controls and neglect patients so that their performance could be compared.
As a final remark, I want to thank Doricchi and colleagues for the interest in our study, for the effort and time needed in recruiting an adequate sample of control subjects, and for correctly and carefully using our procedure to prepare the stimuli, as I have described it to the first author in a personal communication after the publication of our paper. Nonetheless, their data do not refute the results of the first experiment of our study: the discrepancies between the two experiments can be reconciled taking into account the relationship between a strong rightward bias with long lines and a strong leftward bias with short lines. Moreover, regardless of the discrepancy between their results and ours, we do not believe that they constitute a ‘confutation of the space anisometry hypothesis interpretation of neglect and cross-over’ as a study on the performance of healthy individuals cannot refute a hypothesis about the clinical syndrome of neglect. If we might refute a theory only on the basis of the behaviour of healthy subjects, we would not need to study neglect patients, which would be certainly easier but much less intriguing and informative.
In the same vein, the importance, if any, of our paper to corroborating the space anisometry hypothesis as an explanation of the crossover effect in neglect is much more related to the results of the four experiments with 21 neglect patients other than to the first experiment with five healthy individuals. In that regard, our findings of the crossover effect in patients without hemianopia demonstrate that contralesional fixations to compensate for hemianopia cannot provide an adequate explanation for the effects we observe. Rather, taken as a whole, we believe that the converging results of the five studies presented in our paper provide strong evidence for the space anisometry hypothesis.
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